Convergent transcriptional specializations in the brains of humans and song-learning birds
Open accessAbstract
Song-learning birds and humans share independently evolved similarities in brain pathways for vocal learning that are essential for song and speech and are not found in most other species. Comparisons of brain transcriptomes of song-learning birds and humans relative to vocal nonlearners identified convergent gene expression specializations in specific song and speech brain regions of avian vocal learners and humans. The strongest shared profiles relate bird motor and striatal song-learning nuclei, respectively, with human laryngeal motor cortex and parts of the striatum that control speech production and learning. Most of the associated genes function in motor control and brain connectivity. Thus, convergent behavior and neural connectivity for a complex trait are associated with convergent specialized expression of multiple genes.
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Written from the paper’s full text.
TL;DR
The paper compares brain transcriptomes of vocal-learning birds and humans and identifies convergent gene expression specializations in song and speech brain regions, especially songbird RA with human laryngeal motor cortex and Area X with human putamen/caudate. It argues that convergent vocal-learning behavior and neural connectivity are accompanied by convergent specialized expression of multiple genes.
Key findings
- Dynamic programming alignment of anatomical gene expression specialization trees found songbird Area X best aligned to human putamen, ventral striatum to human nucleus accumbens, and RA to the human central sulcus within primary motor cortex (PrG_cs); HVC and LMAN aligned weakly to cingulate cortex, with their highest hypothesized matches to Wernicke’s and Broca’s areas but without significant permutation/FWER support.
- Statistical tests confirmed Area X–putamen and RA–PrG_cs similarities; 288 genes contributed to shared avian–human striatum specialization, 342 to avian pallium–human cortex, 78 to Area X–putamen, 40 to RA–PrG_cs, and 55 mostly nonoverlapping genes (only 3 overlapping with the 40) to RA analogs–human LMC/dLSC.
- Across all three vocal-learning avian lineages (songbird, parrot, hummingbird), RA analogs showed stronger convergent specialization with human LMC/dLSC than vocal-nonlearning dove/quail arcopallium; 55 genes were identified, with ~91% decreased expression in RA analogs and human LMC/dLSC, and in situ hybridization of 15 genes gave ~95% true positive rate for differential expression in zebra finch RA.
- Proteomics identified 81 proteins differentially expressed in zebra finch RA; mRNA–protein correlation was modest but significant (R² = 0.18, P = 9.4 × 10⁻⁵), and top disease categories included movement disorders (P = 8.7 × 10⁻¹⁴, 29 genes).
Methods
- Six experiments were analyzed: laser-microdissected song nuclei from zebra finches; microarray samples of Area X and ventral striatum; RA analogs and adjacent motor arcopallium across vocal-learning and vocal-nonlearning birds; brainstem vocal and neck motor neurons; 3702 human samples from 231 subregions of six Allen Human Brain Atlas subjects; and 258 macaque cortical-layer samples from 12 regions of four rhesus macaques.
- Avian samples used a custom zebra finch Agilent oligoarray v2.2; human samples used a human Agilent 8×60K array containing 7473 human–finch orthologous genes; cross-species avian filtering yielded 3044 genes for multi-lineage comparisons, and macaque comparisons used 4702 orthologs.
- Analyses included anatomical gene expression specialization trees, pairwise distances and Pearson correlations, a dynamic programming alignment preserving hierarchical structure, permutation/FWER tests, linear regression to count shared specialized genes, functional enrichment, in situ hybridization, and nanoscale capillary tandem mass spectrometry.
Limitations
- The paper states that correlations were low even between biological replicates (mean zebra finch RA vs. adjacent mAC replicate correlation = 0.22), that the analyses do not show the specializations are functionally related to projections or vocal learning and could be a consequence rather than a cause, that HVC/LMAN convergent specializations were not significant, that human premortem vocalizing state was unknown, that brainstem vocal/neck motor neurons could not be aligned to proposed human homologs because they were not isolated in the Allen data, and that macaque data were limited in regions, cortical layers, and ortholog number.
- Evident from the text: cross-species microarray orthology and filtering may miss genes; human samples were collected 10 to 30 hours postmortem, which may affect RNA profiles; avian samples were from silent adult males, limiting behavioral-state and sex coverage; and no causal manipulation tests gene function in vocal learning.
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Claims the paper makes
0 of 97 cited sources checked · 0 supported · 0 flagged
- Findingown data
The mean correlation between biological replicates of zebra finch RA relative to the adjacent mAC specialization is 0.22.
“For example, the mean correlation between biological replicates of zebra finch RA relative to the adjacent mAC specialization is 0.22.”
Quote in the paperNot a substantial claim - Findingown data
The dynamic programming algorithm found an optimal alignment between the brain gene expression specialization trees of songbird and human.
“The dynamic programming algorithm found an optimal alignment between the brain gene expression specialization trees of songbird (Fig. 2A) and human (Fig. 2B; see also Table 1).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Songbird striatal regions (Area X and VS) were confirmed by both methods to have the most similar specialized gene expression to the human striatum.
“In particular, songbird striatal regions (Area X and VS) were confirmed by both methods to have the most similar specialized gene expression to the human striatum (Fig. 3A and fig. S3A; Table 1 and table S3A).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The mAC lateral to RA, which does not participate in song production and does not make direct projections, aligned weakly to human superior rostral gyrus of frontal lobe.
“The mAC lateral to RA, which does not participate in song production (9, 51) and does not make direct projections (52, 53), aligned weakly to the human superior rostral gyrus (SRoG) of the frontal lobe (Fig. 2B).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Pearson correlations between specializations were low, even in biological replicates, because of noise and large numbers of genes that are not specialized in expression.
“We found that the Pearson correlations between specializations were low, even in biological replicates, because of noise and large numbers of genes that are not specialized in expression.”
Quote in the paperSubstantial claim
- Findingnone given
Values above 0.09 were typically statistically significant.
“Values above 0.09 were typically statistically significant (see below).”
Quote in the paperNot a substantial claim - Findingown data
The closest match for nXIIts in the available human data was to the vagus motor neurons (n10).
“However, the closest match for nXIIts in the available human data was to the vagus motor neurons (n10) (Fig. 2B and Table 1).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Avian ventral striatum adjacent to Area X that does not participate in vocal learning best aligned to human ventral striatum (nucleus accumbens ventral to putamen).
“The avian ventral striatum (VS) adjacent to Area X that does not participate in vocal learning best aligned to the human ventral striatum [i.e., nucleus accumbens (Acb) ventral to the putamen] (Fig. 2B).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Songbird Area X best aligned to human putamen.
“At lower levels of the tree alignment (individual brain regions), songbird Area X best aligned to the human putamen (Pu) (Fig. 2B and Table 1), supporting a prediction made on the basis of other evidence (41, 44, 48).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The songbird vocal (nXIIts) and neck (SSp) motor neurons could not be aligned to their proposed human homologs because they were not isolated as part of the Allen Human Brain Atlas data set.
“Within the brainstem, the songbird vocal (nXIIts) and neck (SSp) motor neurons could not be aligned to their proposed human homologs—the nucleus ambiguus and supraspinal nucleus, respectively (16, 44, 49, 54)—because they were not isolated as part of the Allen Human Brain Atlas data set.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Songbird RA best aligned to human central sulcus (PrG_cs) within primary motor cortex.
“Songbird RA best aligned to the human central sulcus (PrG_cs) within the primary motor cortex [i.e., within the precentral gyrus (PrG)] (Fig. 2B), supporting a prediction of the cortex hypothesis (4, 33, 41, 49);”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Both permutation and gene number methods gave moderate to strong statistical support for most zebra finch and human regions aligned by the dynamic programming algorithm at Pearson correlations of ~0.09 and above.
“Both the permutation and gene number methods gave moderate (P ≈ 0.05) to strong (P < 0.001) statistical support for most zebra finch and human regions aligned by the dynamic programming algorithm at Pearson correlations of ~0.09 and above (Fig. 2B, Table 1, and fig. S3).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The zebra finch RA specialization best matched specific samples at or near coordinates of a recently hypothesized dorsal LMC (dLMC) and adjacent somatosensory laryngeal cortex (dLSC) within PrG and PoG, as well as to vLMC samples within PrG, all regions that have the highest functional activation during speech production.
“Similarly, the zebra finch RA specialization best matched specific samples at or near coordinates of a recently hypothesized dorsal LMC (dLMC) and adjacent somatosensory laryngeal cortex (dLSC) (62, 63) within the PrG and PoG, respectively, as well as to vLMC samples within PrG, all regions that have the highest functional activation during speech production (Fig. 4B) (59).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The reduced set of genes recapitulated the strong relationship between gene expression specializations in zebra finch RA and human PrG_cs.
“This reduced set of genes applied to our dynamic programming algorithm recapitulated the strong relationship between gene expression specializations in zebra finch RA and human PrG_cs (fig. S4A).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
A significant number of genes overlapped between the human LMC/dLSC and the vocal-learning minus vocal-nonlearning birds.
“A significant number of genes overlapped between the human LMC/dLSC and the vocal-learning minus vocal-nonlearning birds (Fig. 3, E and F, permutation test; Table 1).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Another region proposed to be functionally analogous to RA, the cingulate gyrus, also had strong similarity from both tests.
“Another region proposed to be functionally analogous to RA, the cingulate gyrus (4), also had strong similarity from both tests (Fig. 3D and fig. S3D; Table 1 and table S3D).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The relationship between RA analog and human PrG_cs was stronger for the RA analog of all three vocal learners relative to the similarly located central arcopallium of both vocal nonlearners.
“This relationship was stronger for the RA analog of all three vocal learners (fig. S4, A to C) relative to the similarly located central arcopallium of both vocal nonlearners (fig. S4, D and E).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingcitation
Several human samples with the highest molecular scores shared with songbird RA are in proximity to the center of a region activated during production of vowels, as opposed to production of tongue, lip, or jaw movements.
“Moreover, several of the human samples with the highest molecular scores shared with songbird RA, which controls the syrinx and not the tongue, beak, or jaw (41), are in proximity to the center of a region activated during the production of vowels (generated by the LMC connections to the larynx), as opposed to the production of tongue, lip, or jaw movements (Fig. 4B) (59).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
288 genes contributed significantly to the shared specialization between the avian and human striatum.
“We found that 288 genes contributed significantly to the shared specialization between the avian and human striatum (table S3A).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The vector of genes and expression levels in all vocal-learning birds had a positive correlation with genes specialized in LMC/dLSC relative to the surrounding PrG and PoG (0.14, permutation P = 0.016).
“This vector of genes and expression levels in all vocal-learning birds had a positive correlation with genes specialized in LMC/dLSC relative to the surrounding PrG and PoG (0.14, permutation P = 0.016).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The zebra finch Area X specialization best matched specific human putamen and caudate samples that overlapped and extended with the coordinates of brain regions activated during speech production.
“We found that the zebra finch Area X specialization best matched specific human putamen and caudate samples that overlapped and extended with the coordinates of brain regions activated during speech production (Fig. 4A) (56–58).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Songbird RA had the highest match to layer 5 cells of macaque primary motor cortex (with a secondary match to layer 5 of premotor cortex) relative to all other layers within the primary motor cortex and to all layers of all other cortical regions sampled.
“All of our approaches (correlation, gene number, and permutation) showed that songbird RA had the highest match to layer 5 cells of macaque primary motor cortex (with a secondary match to layer 5 of premotor cortex) relative to all other layers within the primary motor cortex and to all layers of all other cortical regions sampled (cingulate, auditory, visual, and other cortices; Table 1, fig. S5,”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
HVC had the best match, although weaker, to macaque layer 2 of the PoG and other cortical regions.
“HVC had the best match, although weaker, to macaque layer 2 of the PoG and other cortical regions (Table 1, fig. S5, C and D, and table S3H).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
342 genes contributed to the shared specialization between avian pallium and human cortex.
“Similarly, 342 genes contributed to the shared specialization between avian pallium and human cortex, and also included those validated by in situ hybridization (fig. S6, C and D, and table S3B) (43).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Functional enrichment analysis of these genes found movement disorders (68 genes) and disorders of the basal ganglia (55 genes) as two of the top categories.
“Functional enrichment analysis of these genes found movement disorders (68 genes) and disorders of the basal ganglia (55 genes) as two of the top categories (table S5A), consistent with known functions of the striatum.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
There is a strong similarity in gene expression between PrG and PoG samples.
“This is supported by a strong similarity in gene expression between PrG and PoG samples (fig. S2C).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingcitation
Only the core portion of the parrot RA analog showed SLIT1 down-regulation.
“Only the core portion of the parrot RA analog showed SLIT1 down-regulation (Fig. 6A) (70).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [70] Wang R Convergent differential regulation of ROBO-SLIT axon guidance pathway genes in the brains of vocal learners J Comp Neurol 10.1002/cne.23719 2014 PMC4329046 25424606 source
Not checked in the free run.
- Findingown data
SLIT1 was partially down-regulated in the adjacent mAC of zebra finches.
“it was also partially down-regulated in the adjacent mAC of zebra finches”
Quote in the paperNot a substantial claim - Findingown data
The top enrichment categories for Area X-putamen shared genes were movement disorders (21 genes) and ataxia (8 genes).
“The top enrichment categories were movement disorders (21 genes) and ataxia (8 genes; table S5C), consistent with motor-driven neural activity and gene regulation in Area X (4, 42), and with functional magnetic resonance activation during speech production in the matching human striatal regions (57).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
A mostly nonoverlapping set of 55 genes (only 3 overlapping) contributed to the convergent shared specialized expression between the RA analogs of vocal learners and human LMC/dLSC.
“In contrast, we found a mostly nonoverlapping set of 55 genes (only 3 overlapping) that contributed to the convergent shared specialized expression between the RA analogs of vocal learners and human LMC/dLSC (Fig. 5 and table S6).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
SLIT1 showed verified down-regulation in the RA analog of all vocal-learning bird species.
“SLIT1, which showed verified down-regulation in the RA analog of all vocal-learning bird species”
Quote in the paperSubstantial claim - Findingown data
78 genes contributed significantly to the shared specialized expression between songbird Area X and human putamen.
“We identified 78 genes that contributed significantly to the shared specialized expression between songbird Area X and human putamen (fig. S7 and table S3C).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Marmosets have lower SLIT1 in primary motor cortex.
“which we also found in marmosets (fig. S13)”
Quote in the paperNot a substantial claim - Findingown data
Area 6v in nonhuman primates did not show differential expression of SLIT1.
“did not show differential expression of SLIT1 (fig. S13)”
Quote in the paperSubstantial claim - Findingown data
In situ hybridization analyses of 13 randomly selected genes revealed that those with a permutation P < 0.015 had a true positive rate of ~90% for differential expression in Area X.
“In situ hybridization analyses of 13 randomly selected genes revealed that those with a permutation P < 0.015 had a true positive rate of ~90% for differential expression in Area X (fig. S7, highlighted genes, fig. S8, and table S3C).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
SLIT1 showed no down-regulation in the arcopallium of vocal-nonlearning species.
“but no down-regulation in the arcopallium of the vocal-nonlearning species”
Quote in the paperSubstantial claim - Findingown data
In situ hybridization of 15 of the 55 genes revealed a ~95% true positive rate for differential expression in zebra finch RA relative to one or more parts of the adjacent arcopallium.
“In situ hybridization of 15 of the 55 genes (selected because of their axon guidance functions or previously published profiles) revealed a ~95% true positive rate for differential expression in zebra finch RA relative to one or more parts of the adjacent arcopallium (Fig. 6, figs. S9 and S10, and table S5).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
The majority of identified genes (50 genes; ~91%) had decreased expression in the RA analogs and human LMC/dLSC relative to the surrounding regions, as opposed to only four that had increased levels.
“The majority of identified genes (50 genes; ~91%) had decreased expression in the RA analogs and human LMC/dLSC relative to the surrounding regions, as opposed to only four that had increased levels (Fig. 6).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Findingown data
Putative human dLMC in the central sulcus showed further down-regulation of SLIT1, particularly in the upper cortical layers.
“our putative human dLMC in the central sulcus showed further down-regulation, particularly in the upper cortical layers”
Quote in the paperSubstantial claim - Findingown data
NEUROD6 was weakly down-regulated in zebra finch RA.
“Although weakly down-regulated in zebra finch RA”
Quote in the paperNot a substantial claim - Findingown data
Genes with lower mRNA expression in RA showed a stronger correlation with protein levels (P = 0.006).
“the genes that had lower mRNA expression in RA showed a stronger correlation with protein levels (t test, P = 0.006; fig. S16B)”
Quote in the paperNot a substantial claim - Findingown data
Negative control genes, including SLIT2, did not show differential expression in RA analogs and human LMC.
“We examined negative control genes, some belonging to the same gene families (such as SLIT2), and did not find differential expression in RA analogs (70) and human LMC (Fig. 7).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [70] Wang R Convergent differential regulation of ROBO-SLIT axon guidance pathway genes in the brains of vocal learners J Comp Neurol 10.1002/cne.23719 2014 PMC4329046 25424606 source
Not checked in the free run.
- Findingown data
Top disease categories for protein analyses included movement disorders (P = 8.7 × 10−14, 29 genes), neural connectivity, and brain development.
“the top disease categories for the protein analyses included movement disorders (P = 8.7 × 10−14, 29 genes), and other categories included neural connectivity and brain development (table S5F)”
Quote in the paperNot a substantial claim - Findingown data
SLIT1, NEUROD6, C1QL3, and PVALB are among the most differentially expressed genes in dLMC and RA of both species, among all 7473 orthologs.
“SLIT1, NEUROD6, C1QL3, and PVALB being among the most differentially expressed genes in the dLMC and RA of both species (fig. S15)”
Quote in the paperSubstantial claim - Findingown data
GAP43, SNCA, and UCHL1 were down-regulated proteins also identified in mRNA analyses for avian RA and human LMC.
“Three of the specialized down-regulated proteins, GAP43, SNCA, and UCHL1, were also identified in the mRNA analyses for avian RA and human LMC.”
Quote in the paperSubstantial claim - Findingown data
Top biological pathway gene ontology category overall was endocytosis of vesicles involved in cellular assembly and organization (P = 6.6 × 10−11, 7 genes).
“The top biological pathway gene ontology category overall was endocytosis of vesicles involved in cellular assembly and organization (P = 6.6 × 10−11, 7 genes)”
Quote in the paperNot a substantial claim - Findingown data
The pattern of NEUROD6 down-regulation in putative human dLMC was distinct such that it defined the boundaries of the region.
“the pattern of down-regulation in the putative human dLMC was distinct such that it defined the boundaries of the region (Fig. 7)”
Quote in the paperSubstantial claim - Findingown data
In mouse putative rudimentary LMC, 10 candidate genes did not show differential expression, except PVALB with reduced expression.
“did not identify examples of differential expression (fig. S14), except for PVALB but with reduced expression (fig. S14)”
Quote in the paperNot a substantial claim - Findingown data
Individual mRNA and protein level differences in RA and surrounding arcopallium had a modest but significant correlation (R2 = 0.18, P = 9.4 × 10−5).
“individual mRNA and protein level differences in RA and the surrounding arcopallium had a modest but significant correlation (R2 = 0.18, P = 9.4 × 10−5)”
Quote in the paperSubstantial claim - Findingown data
81 proteins were differentially expressed in RA.
“We identified 81 proteins as differentially expressed in RA (fig. S16A)”
Quote in the paperSubstantial claim - Findingown data
FOXP2 showed lower expression in the dLMC region.
“FOXP2 showed lower expression in the dLMC region (fig. S12)”
Quote in the paperSubstantial claim - Findingown data
Corresponding mRNA gene expression differences were detected in the microarray experiment.
“detected corresponding mRNA gene expression differences in the microarray experiment (table S7)”
Quote in the paperSubstantial claim - Findingnone given
Enriched neurotransmission functions of convergently specialized genes in songbird Area X and parts of human putamen/caudate.
“The enriched neurotransmission functions of the convergently specialized genes in songbird Area X and parts of the human putamen/caudate”
Quote in the paperSubstantial claim - Findingown data
Lack of finding significant convergent specializations of songbird HVC or LMAN with humans.
“Our lack of finding significant convergent specializations of the songbird HVC or LMAN with humans”
Quote in the paperSubstantial claim - Premisecitation
Vocal learning convergently evolved in a few lineages of mammals and birds, including humans, cetaceans, pinnipeds, bats, elephants, songbirds, parrots, and hummingbirds.
“Vocal learning is the ability to learn to produce vocalizations by imitating a model. This complex trait convergently evolved in a few lineages of mammals and birds (fig. S1). These include humans, cetaceans (whales and dolphins), pinnepeds (seals and sea lions), bats, and elephants among mammals, and songbirds, parrots, and hummingbirds among birds (1).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [1] Petkov CI Jarvis ED Birds, primates, and spoken language origins: Behavioral phenotypes and neurobiological substrates Front Evol Neurosci 4 12 2012 10.3389/fnevo.2012.00012 22912615 PMC3419981
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- Premisecitation
No strong evidence exists that nonhuman primates learn novel vocalizations.
“Although nonhuman primates have a limited ability to modify their innate vocalizations, no strong evidence exists that they learn novel vocalizations (1–3).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [1] Petkov CI Jarvis ED Birds, primates, and spoken language origins: Behavioral phenotypes and neurobiological substrates Front Evol Neurosci 4 12 2012 10.3389/fnevo.2012.00012 22912615 PMC3419981
Not checked in the free run.
- cites [2] Jürgens U The neural control of vocalization in mammals: A review J Voice 23 1 10 2009 10.1016/j.jvoice.2007.07.005; 18207362
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- cites [3] Egnor SE Hauser MD A paradox in the evolution of primate vocal learning Trends Neurosci 27 649 654 2004 10.1016/j.tins.2004.08.009 15474164
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- Premisecitation
Functional brain region specializations in song-learning birds and humans are associated with some molecular specializations.
“These functional brain region specializations in song-learning birds (12–17) and in humans (18) are associated with some molecular specializations.”
Quote in the paperSubstantial claim0 of 7 sources checked- cites [12] Lovell PV Clayton DF Replogle KL Mello CV Birdsong “transcriptomics”: Neurochemical specializations of the oscine song system PLOS ONE 3 e3440 2008 10.1371/journal.pone.0003440 18941504 PMC2563692
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- cites [13] Lovell PV Carleton JB Mello CV Genomics analysis of potassium channel genes in songbirds reveals molecular specializations of brain circuits for the maintenance and production of learned vocalizations BMC Genomics 14 470 2013 10.1186/1471-2164-14-470 23845108 PMC3711925
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- cites [14] Matsunaga E Suzuki K Kobayashi T Okanoya K Comparative analysis of mineralocorticoid receptor expression among vocal learners (Bengalese finch and budgerigar) and non-vocal learners (quail and ring dove) has implications for the evolution of avian vocal learning Dev Growth Differ 53 961 970 2011 10.1111/j.1440-169X.2011.01302.x 22010640
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- cites [15] Hilliard AT Miller JE Horvath S White SA Distinct neurogenomic states in basal ganglia subregions relate differently to singing behavior in songbirds PLOS Comput Biol 8 e1002773 2012 10.1371/journal.pcbi.1002773 23144607 PMC3493463
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- cites [16] Hara E Rivas MV Ward JM Okanoya K Jarvis ED Convergent differential regulation of parvalbumin in the brains of vocal learners PLOS ONE 7 e29457 2012 10.1371/journal.pone.0029457 22238614 PMC3253077
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- cites [17] Horita H Specialized motor-driven dusp1 expression in the song systems of multiple lineages of vocal learning birds PLOS ONE 7 e42173 2012 10.1371/journal.pone.0042173 22876306 PMC3410896
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- cites [18] Amunts K Broca’s region: Novel organizational principles and multiple receptor mapping PLOS Biol 8 e1000489 2010 10.1371/journal.pbio.1000489 20877713 PMC2943440 source
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- Premisecitation
The gene encoding parvalbumin shares specialized expression in brainstem vocal-oral nuclei between song-learning birds and humans.
“One gene, encoding parvalbumin, was found to share specialized expression in brainstem vocal-oral nuclei between song-learning birds and humans (16).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [16] Hara E Rivas MV Ward JM Okanoya K Jarvis ED Convergent differential regulation of parvalbumin in the brains of vocal learners PLOS ONE 7 e29457 2012 10.1371/journal.pone.0029457 22238614 PMC3253077
Not checked in the free run.
- Premisecitation
The human central sulcus and songbird RA have some of the most robust direct projections to brainstem motor neurons known.
“the human central sulcus and songbird RA have some of the most robust direct projections to brainstem motor neurons known (Fig. 1) (41, 50).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [41] Jarvis ED Learned birdsong and the neurobiology of human language Ann NY Acad Sci 1016 749 777 2004 10.1196/annals.1298.038 15313804 PMC2485240
Not checked in the free run.
- cites [50] Rathelot JA Strick PL Subdivisions of primary motor cortex based on cortico-motoneuronal cells Proc Natl Acad Sci USA 106 918 923 2009 10.1073/pnas.0808362106 19139417 PMC2621250
Not checked in the free run.
- Interpretationown data
The avian RA analogs of each vocal-learning lineage have mostly the same convergent molecular specializations with human LMC/dLSC.
“Overall, these findings indicate that the avian RA analogs of each vocal-learning lineage have mostly the same convergent molecular specializations with human LMC/dLSC.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Interpretationreasoning
The match of RA to LMC/dLSC contributed to the relationship of RA with the broader human primary motor cortex.
“The results suggest that the match of RA to LMC/dLSC contributed to the relationship of RA with the broader human primary motor cortex.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Interpretationreasoning
The specialized genes could play a role in mediating the differential connectivity of avian RA and of human LMC.
“The latter finding suggests that the specialized genes could play a role in mediating the differential connectivity of avian RA and of human LMC.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
- Premisecitation
Macaques have lower SLIT1 in primary motor cortex.
“macaques have recently been shown to have lower SLIT1 in primary motor cortex (69)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [69] Sasaki T Komatsu Y Watakabe A Sawada K Yamamori T Prefrontal-enriched SLIT1 expression in Old World monkey cortex established during the postnatal development Cereb Cortex 20 2496 2510 2010 10.1093/cercor/bhp319 20123755 PMC2936805
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- Premisecitation
In parrots, the RA analog core portion makes a direct projection to brainstem vocal motor neurons.
“the RA analog has a core portion that makes a direct projection to brainstem vocal motor neurons”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [70] Wang R Convergent differential regulation of ROBO-SLIT axon guidance pathway genes in the brains of vocal learners J Comp Neurol 10.1002/cne.23719 2014 PMC4329046 25424606 source
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- Premisecitation
Area 6v is not required for vocalization.
“this region is not required for vocalization (61)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [61] Simonyan K Horwitz B Laryngeal motor cortex and control of speech in humans Neuroscientist 17 197 208 2011 10.1177/1073858410386727 21362688 PMC3077440 source
Not checked in the free run.
- Premisecitation
In parrots, the RA analog has a more ventral shell portion unique to parrots that projects to other song nuclei.
“as well as a more ventral shell portion unique to parrots that projects to other song nuclei (70)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [70] Wang R Convergent differential regulation of ROBO-SLIT axon guidance pathway genes in the brains of vocal learners J Comp Neurol 10.1002/cne.23719 2014 PMC4329046 25424606 source
Not checked in the free run.
- Interpretationown data
Behavioral and neuroanatomical convergence for the vocal-learning trait is associated with molecular convergence of gene expression changes in the circuits that control the behavior.
“Our study indicates that behavioral and neuroanatomical convergence for the vocal-learning trait is associated with molecular convergence of gene expression changes in the circuits that control the behavior.”
Quote in the paperSubstantial claim - Interpretationreasoning
The findings support broader homologous brain regions in which these specialized song and speech regions are located.
“and further support broader homologous brain regions in which these specialized song and speech regions are located”
Quote in the paperSubstantial claim - Premisecitation
Avian RA and human primary motor cortex make more direct contacts with vocal motor neurons than do motor cortex neurons in any other vertebrates tested to date.
“the avian RA and human primary motor cortex make more direct contacts with vocal motor neurons than do motor cortex neurons in any other vertebrates tested to date (6, 61)”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [6] Arriaga G Jarvis ED Mouse vocal communication system: Are ultrasounds learned or innate? Brain Lang 124 96 116 2013 10.1016/j.bandl.2012.10.002 23295209 PMC3886250
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- cites [61] Simonyan K Horwitz B Laryngeal motor cortex and control of speech in humans Neuroscientist 17 197 208 2011 10.1177/1073858410386727 21362688 PMC3077440 source
Not checked in the free run.
- Premisecitation
Avian arcopallium, like motor cortex in many mammals, is thought to make mostly indirect contact with lower motor neurons.
“the avian arcopallium, like the motor cortex in many mammals, is thought to make mostly indirect contact with lower motor neurons (6)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [6] Arriaga G Jarvis ED Mouse vocal communication system: Are ultrasounds learned or innate? Brain Lang 124 96 116 2013 10.1016/j.bandl.2012.10.002 23295209 PMC3886250
Not checked in the free run.
- Premisecitation
SLIT1 has an important role in speech and vocal learning.
“Our findings on SLIT1 add to a growing body of studies implicating an important role for this gene in speech and vocal learning.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [71] Konopka G Human-specific transcriptional regulation of CNS development genes by FOXP2 Nature 462 213 217 2009 10.1038/nature08549 19907493 PMC2778075
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- cites [76] Fisher SE Francks C Genes, cognition and dyslexia: Learning to read the genome Trends Cognit Sci 10 250 257 2006 10.1016/j.tics.2006.04.003 16675285
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- cites [32] Wang R thesis Duke University 2011 http://dukespace.lib.duke.edu/dspace/bitstream/handle/10161/5630/Wang_duke_0066D_10911.pdf?sequence=1
Not checked in the free run.
- Interpretationown data
The findings identify specific molecularly analogous brain regions for song and speech between birds and humans.
“The findings identify specific molecularly analogous brain regions for song and speech between birds and humans”
Quote in the paperSubstantial claim - Premisecitation
SLIT1 promoter is a target of the FOXP2 transcription factor.
“SLIT1 promoter is a target of the FOXP2 transcription factor (71)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [71] Konopka G Human-specific transcriptional regulation of CNS development genes by FOXP2 Nature 462 213 217 2009 10.1038/nature08549 19907493 PMC2778075
Not checked in the free run.
- Premisecitation
Direct cortical projections to lower motor neurons are correlated with finer motor control and more complex motor learning.
“Direct cortical projections to lower motor neurons are correlated with finer motor control and more complex motor learning (75).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [75] Lemon RN Descending pathways in motor control Annu Rev Neurosci 31 195 218 2008 10.1146/annurev.neuro.31.060407.125547 18558853 source
Not checked in the free run.
- Interpretationcitation
Our results add to growing body of work that shows dLMC could viably be a specialized part of the speech control circuit.
“our results add to the growing body of work (62) that shows this region could viably be a specialized part of the speech control circuit”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [62] Simonyan K The laryngeal motor cortex: Its organization and connectivity Curr Opin Neurobiol 28 15 21 2014 10.1016/j.conb.2014.05.006 24929930 PMC4177508
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- Premisecitation
SLIT1 was more differentially up-regulated by human FOXP2 than by chimpanzee FOXP2.
“SLIT1 was found to be more differentially up-regulated by the human FOXP2 transcription factor than by the chimpanzee FOXP2 (71).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [71] Konopka G Human-specific transcriptional regulation of CNS development genes by FOXP2 Nature 462 213 217 2009 10.1038/nature08549 19907493 PMC2778075
Not checked in the free run.
- Premisecitation
SLIT1 is a ligand for the ROBO1 axon guidance receptor.
“SLIT1 is a ligand for the ROBO1 axon guidance receptor”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [76] Fisher SE Francks C Genes, cognition and dyslexia: Learning to read the genome Trends Cognit Sci 10 250 257 2006 10.1016/j.tics.2006.04.003 16675285
Not checked in the free run.
- Premisecitation
ROBO1 was differentially expressed in fetal human speech brain regions and in the RA analog of avian vocal learners.
“ROBO1 itself was also found to be differentially expressed in fetal human speech brain regions (77) and in the RA analog of avian vocal learners (70).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [77] Johnson MB Functional and evolutionary insights into human brain development through global transcriptome analysis Neuron 62 494 509 2009 10.1016/j.neuron.2009.03.027 19477152 PMC2739738 source
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- cites [70] Wang R Convergent differential regulation of ROBO-SLIT axon guidance pathway genes in the brains of vocal learners J Comp Neurol 10.1002/cne.23719 2014 PMC4329046 25424606 source
Not checked in the free run.
- Premisecitation
ROBO1 is one of five candidate genes with convergent amino acid substitutions in vocal-learning mammals.
“ROBO1 is one of five candidate genes with convergent amino acid substitutions in vocal-learning mammals (32).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [32] Wang R thesis Duke University 2011 http://dukespace.lib.duke.edu/dspace/bitstream/handle/10161/5630/Wang_duke_0066D_10911.pdf?sequence=1
Not checked in the free run.
- Premisecitation
Area X does not appear to have large differences in neural connectivity relative to the surrounding striatum.
“Area X does not appear to have large differences in neural connectivity relative to the surrounding striatum (82)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [82] Doupe AJ Perkel DJ Reiner A Stern EA Birdbrains could teach basal ganglia research a new song Trends Neurosci 28 353 363 2005 10.1016/j.tins.2005.05.005 15935486 source
Not checked in the free run.
- Premisecitation
RA neurons have a higher spontaneous firing rate than the surrounding arcopallium.
“the RA neurons have a higher spontaneous firing rate than the surrounding arcopallium (81)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [81] Adret P Margoliash D Metabolic and neural activity in the song system nucleus robustus archistriatalis: Effect of age and gender J Comp Neurol 454 409 423 2002 10.1002/cne.10459 12455006
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- Premisecitation
Companion study found convergent mutations in genomic regulatory regions of some genes with specialized expression in RA analog across vocal-learning lineages.
“in our companion study we found convergent mutations in the genomic regulatory regions of some of the genes we find here with specialized expression in the RA analog across vocal-learning lineages (33)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [33] Zhang G Comparative genomics reveals insights into avian genome evolution and adaptation Science 346 1311 1320 2014 10.1126/science.1251385 25504712 PMC4390078
Not checked in the free run.
- Interpretationown data
Our experiments provide a candidate set of genes involved in neural connectivity and cell communication functions.
“Our experiments provide a candidate set of genes involved in neural connectivity and cell communication functions.”
Quote in the paperSubstantial claim - Interpretationreasoning
Brain circuits for complex traits may have limited ways in which they could have evolved from a common ancestor.
“indicates that brain circuits for complex traits may have limited ways in which they could have evolved from a common ancestor”
Quote in the paperSubstantial claim - Interpretationown data
Convergent neural circuits for vocal learning are accompanied by convergent molecular changes of multiple genes in species separated by millions of years from a common ancestor.
“The fact that convergent neural circuits for vocal learning are accompanied by convergent molecular changes of multiple genes in species separated by millions of years from a common ancestor”
Quote in the paperSubstantial claim - Interpretationreasoning
Gene expression similarities across species, combined with circuit and functional similarities, suggest that avian vocal learners can be used as models for speech production at a molecular level.
“The gene expression similarities we find across species, combined with circuit and functional similarities (40, 41), suggest that avian vocal learners can be used as models for speech production at a molecular level.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [40] Brainard MS Doupe AJ Translating birdsong: Songbirds as a model for basic and applied medical research Annu Rev Neurosci 36 489 517 2013 10.1146/annurev-neuro-060909-152826 23750515 PMC4130661
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- cites [41] Jarvis ED Learned birdsong and the neurobiology of human language Ann NY Acad Sci 1016 749 777 2004 10.1196/annals.1298.038 15313804 PMC2485240
Not checked in the free run.
- Study design and conductown data
Overlap between our Agilent microarray and cDNA microarray was not high enough to incorporate HVC data into our framework.
“the overlap between our Agilent microarray was not high enough to incorporate these data into our framework”
Quote in the paperSubstantial claim - Interpretationown data
Our study has identified molecularly analogous brain regions that function in song and speech in vocal-learning birds and humans.
“Our study has identified molecularly analogous brain regions that function in song and speech in vocal-learning birds and humans.”
Quote in the paperSubstantial claim - Interpretationown data
Our results across species suggest that arcopallium is not similar to mammalian amygdala.
“our results across species suggest that this is not the case for the arcopallium, the region most often suggested to be similar to the mammalian amygdala (34, 44)”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [34] Jarvis ED Avian brains and a new understanding of vertebrate brain evolution Nat Rev Neurosci 6 151 159 2005 10.1038/nrn1606 15685220 PMC2507884
Not checked in the free run.
- cites [44] Reiner A The Avian Brain Nomenclature Forum: Terminology for a new century in comparative neuroanatomy J Comp Neurol 473 E1 E6 2004 19626136 PMC2713747
Not checked in the free run.
- May combine two claims. 39
- Classified as probably not a substantial claim. 14
- The quote only partly states this claim. 2
May combine two claims.
Findingown dataAvian pallial regions were confirmed to be most similar to human cortex, with lower significance by permutation analyses (P = 0.068) and FWER analyses (0.218) but with the highest number of specialized genes in common of all regions compared.
“The avian pallial regions were confirmed to be most similar to the human cortex, with a lower significance by the permutation analyses (P = 0.068) and corresponding FWER analyses (0.218) but with the highest number of specialized genes in common of all regions compared (Fig. 3B and fig. S3B; Table 1 and table S3B).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataBoth HVC and LMAN aligned best to the parietal part of the cingulate cortex, but the correlations were low.
“Both HVC and LMAN aligned best to the parietal part of the cingulate cortex, but the correlations were low (Fig. 2B).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataAt high levels of the alignment, songbird telencephalic regions corresponded most closely to human telencephalon and songbird brainstem nuclei corresponded to human brainstem nuclei.
“At high levels of the alignment, the songbird telencephalic regions corresponded most closely to the human telencephalon (Tel) and the songbird brainstem nuclei corresponded to human brainstem nuclei.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataWithin the telencephalon, songbird pallial regions corresponded most closely to human cortex, and songbird striatal regions corresponded to human striatum.
“Within the telencephalon, the songbird pallial regions corresponded most closely to the human cortex (Cx), and the songbird striatal regions corresponded to the human striatum.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataThe songbird pallial regions sampled did not have a strong similarity to human claustrum and had an inverse gene expression relationship with the amygdala.
“The songbird pallial regions sampled did not have a strong similarity to the human claustrum (Cl) and had an inverse gene expression relationship with the amygdala (Amg), meaning that the specialization was in the opposite direction (Table 1).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataOf the regions hypothesized to be similar to HVC or LMAN, the highest correlation values were HVC with Wernicke's auditory speech processing region and LMAN with Broca's speech production and processing region.
“None of the regions hypothesized to be similar to HVC or LMAN had a strong secondary match (correlations > 0.09), but of the hypothesized regions, the highest correlation values were HVC with Wernicke’s auditory speech processing region and LMAN with Broca’s speech production and processing region (Table 1).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataFor HVC and LMAN, of the hypothesized human brain regions, the highest similarities were to Wernicke's area (plus Heschl's and transverse auditory gyri) and Broca's area, respectively, but the relationships were not significant according to permutation and FWER tests.
“For HVC and LMAN, of the hypothesized human brain regions, again the highest similarities were to Wernicke’s area (plus Heschl’s and transverse auditory gyri; HG, TG) and Broca’s area, respectively, but the relationships were not significant according to the permutation and FWER tests (Table 1, fig. S3F, and table S3F).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataThe top enrichment categories for avian pallium-human cortex shared genes were behavior (64 genes) and neurotransmission (38 genes).
“The top enrichment categories were behavior (64 genes) and neurotransmission (38 genes; table S5B).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataThe RA analogs of all three vocal learners had many more genes specialized in common with the human LMC/dLSC than did the arcopallium of vocal nonlearners, and the number of specialized genes in common was significant only for the vocal learners.
“Likewise, the RA analogs of all three vocal learners had many more genes specialized in common with the human LMC/dLSC than did the arcopallium of vocal nonlearners, and the number of specialized genes in common was significant only for the vocal learners (Fig. 3, E and F, and table S4, B and C).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
Probably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataThe common specialized genes between all arcopallium samples of each avian species and the entire human frontal lobe were similar across all avian species.
“For a control analysis, we identified the common specialized genes between all the arcopallium samples of each avian species and the entire human frontal lobe, and found them to be similar across all avian species (Fig. 3G).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataThere was a weak, nonsignificant difference in the correlation between the arcopallium regions of avian vocal learners versus nonlearners and macaque layer 5 cells, but a stronger significant correlation between the RA analogs of avian vocal learners versus nonlearners and human LMC/dLSC versus macaque layer 5 cells.
“Comparing the arcopallium samples from each of the avian species with the specializations of human LMC/dLSC versus macaque layer 5, we found a weak, nonsignificant difference in the correlation between the arcopallium regions of avian vocal learners versus nonlearners and macaque layer 5 cells (table S4D), but a stronger significant correlation between the RA analogs of avian vocal learners versus”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataThe correlations increased for the vocal-learning avian species, but not for the vocal-nonlearning avian species, when comparisons were made to specific human putative LMC (dLMC and vLMC) and dLSC samples within PrG_cs and PoG_cs relative to the cortex.
“The correlations increased for the vocal-learning avian species, but not for the vocal-nonlearning avian species, when comparisons were made to the specific human putative LMC (dLMC and vLMC) and dLSC samples within the PrG_cs and PoG_cs relative to the cortex (fig. S4C, triangles and squares); the correlations were still present when the comparison was relative to only the remaining PrG and PoG (”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataBoth tests confirmed Area X to have the strongest similarity with the putamen but a significant secondary relationship with the adjacent body of the caudate.
“Among the striatal regions, both tests confirmed Area X to have the strongest similarity with the putamen (Fig. 3C and fig. S3C; Table 1 and table S3C) but a significant secondary relationship with the adjacent body of the caudate, consistent with the hypothesis that Area X is similar to adjacent parts of the caudate and putamen (41).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataBoth tests confirmed RA to have the strongest similarity to the central sulcus part of human primary motor cortex (PrG_cs) but also to the adjacent primary somatosensory part of the central sulcus (PoG_cs) and to a region where the ventral LMC is located (PrG_sl).
“Among the pallial regions, both tests confirmed RA to have the strongest similarity to the central sulcus part of the human primary motor cortex (PrG_cs) but also to the adjacent primary somatosensory part of the central sulcus (PoG_cs) and to a region where the ventral LMC is located (PrG_sl) (Fig. 3D and fig. S3D; Table 1 and table S3D).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataLMAN had the best match to layer 4 of the PoG and other cortical regions, contradicting previous hypotheses but consistent with a recent study comparing chicken nidopallium to mouse cortical layers.
“However, LMAN, also part of the nidopallium, had the best match to layer 4 of the PoG and other cortical regions, contradicting previous hypotheses (41, 67) (Table 1, fig. S5, E and F, and table S3I) but consistent with a recent study comparing chicken nidopallium to mouse cortical layers (68).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
The quote only partly states this claim.
Findingown dataThe adjacent dLSC showed striking down-regulation of SLIT1 throughout the region.
“The adjacent dLSC showed striking down-regulation throughout the region (Fig. 7).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe anatomical profiles of the genes fell into three categories: expression specialization in the RA analog and human dLMC/dLSC cortex; expression specialization in the RA plus immediately adjacent intermediate arcopallium and LMC plus the adjacent human primary motor cortex; and a more varied pattern of expression within the avian or human brain, but with local differences in avian RA and human
“The anatomical profiles of the genes fell into three categories (Fig. 6 and figs. S9 and S10): (i) those with expression specialization in the RA analog and human dLMC/dLSC cortex; (ii) those with expression specialization in the RA plus immediately adjacent intermediate arcopallium and LMC plus the adjacent human primary motor cortex; and (iii) those with a more varied pattern of expression”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataThe top enrichment categories among the 40 genes shared with motor cortex cells were movement disorders and abnormal morphology of neurons, whereas the 55 genes shared more specifically with LMC/dLSC were related to cognitive behaviors and development of neural connections for different gene subsets.
“The top enrichment categories among the 40 genes shared with motor cortex cells were movement disorders and abnormal morphology of neurons (table S5D), whereas the 55 genes shared more specifically with LMC/dLSC were related to cognitive behaviors (cognition, learning, and memory) and development of neural connections (neuritogenesis, axon and dendrite growth) for different gene subsets (5 to 15”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims. The quote only partly states this claim.
Findingown dataIn contrast to Area X and the analogous putamen/caudate regions, where more than 70% of the genes had increased expression, the majority of RA/LMC/dLSC genes had decreased expression.
“This is in contrast to Area X and the analogous putamen/caudate regions, where more than 70% of the genes had increased expression (fig. S7).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown dataAlthough there was a possible stronger relationship of RA with the speech-dominant left LMC/dLSC hemisphere, the right hemisphere was also correlated.
“On the basis of these results, we analyzed a subset of 10 of the 15 genes by in situ hybridization in our predicted dLMC/dLSC region of the other hemisphere (right) of two human brain specimens used for the microarrays; although we noted a possible stronger relationship of RA with the speech-dominant left LMC/dLSC hemisphere, the right hemisphere was also correlated (SM8).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Findingown data40 genes contributed to the shared specialized expression between songbird RA and human PrG_cs; a subset of these (10 genes) contributed ~50% to the shared specialization between songbird RA and macaque layer 5 of motor cortex.
“We identified 40 genes that contributed to the shared specialized expression between songbird RA and human PrG_cs (table S3D); a subset of these (10 genes) contributed ~50% to the shared specialization between songbird RA and macaque layer 5 of motor cortex (table S3D).”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
Probably not a substantial claim: may not pass S3 (load-bearing).
FindingcitationFOXP2 was up-regulated in layer 5 cells of primary motor cortex (M1) in mouse.
“FOXP2 was also in the opposite direction, with up-regulation in layer 5 cells of primary motor cortex (M1; fig. S14) (73).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [73] Hisaoka T Nakamura Y Senba E Morikawa Y The forkhead transcription factors, Foxp1 and Foxp2, identify different subpopulations of projection neurons in the mouse cerebral cortex Neuroscience 166 551 563 2010 10.1016/j.neuroscience.2009.12.055 20040367
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May combine two claims.
Premiseown dataSong-learning birds and humans share independently evolved similarities in brain pathways for vocal learning that are essential for song and speech and are not found in most other species.
“Song-learning birds and humans share independently evolved similarities in brain pathways for vocal learning that are essential for song and speech and are not found in most other species.”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [1] Petkov CI Jarvis ED Birds, primates, and spoken language origins: Behavioral phenotypes and neurobiological substrates Front Evol Neurosci 4 12 2012 10.3389/fnevo.2012.00012 22912615 PMC3419981
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- cites [4] Doupe AJ Kuhl PK Birdsong and human speech: Common themes and mechanisms Annu Rev Neurosci 22 567 631 1999 10.1146/annurev.neuro.22.1.567 10202549
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- cites [5] Bolhuis JJ Okanoya K Scharff C Twitter evolution: Converging mechanisms in birdsong and human speech Nat Rev Neurosci 11 747 759 2010 10.1038/nrn2931 20959859
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- cites [6] Arriaga G Jarvis ED Mouse vocal communication system: Are ultrasounds learned or innate? Brain Lang 124 96 116 2013 10.1016/j.bandl.2012.10.002 23295209 PMC3886250
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PremisecitationVocal-learning species share babbling, deafness-induced deterioration of learned vocalizations, dialects, and forebrain circuits that control production and learning of vocalizations.
“Vocal-learning species also share the presence of babbling, deafness-induced deterioration of learned vocalizations, dialects, and forebrain circuits that control production and learning of vocalizations (1, 4–6).”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [1] Petkov CI Jarvis ED Birds, primates, and spoken language origins: Behavioral phenotypes and neurobiological substrates Front Evol Neurosci 4 12 2012 10.3389/fnevo.2012.00012 22912615 PMC3419981
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- cites [4] Doupe AJ Kuhl PK Birdsong and human speech: Common themes and mechanisms Annu Rev Neurosci 22 567 631 1999 10.1146/annurev.neuro.22.1.567 10202549
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- cites [5] Bolhuis JJ Okanoya K Scharff C Twitter evolution: Converging mechanisms in birdsong and human speech Nat Rev Neurosci 11 747 759 2010 10.1038/nrn2931 20959859
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- cites [6] Arriaga G Jarvis ED Mouse vocal communication system: Are ultrasounds learned or innate? Brain Lang 124 96 116 2013 10.1016/j.bandl.2012.10.002 23295209 PMC3886250
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Probably not a substantial claim: may not pass S1 (asserted).
PremisecitationFor vocal learning, it has been hypothesized that superregions of a motor learning or auditory perception pathway specialized into subregions that control production of learned vocalizations.
“For vocal learning, it has been hypothesized that the superregions of a motor learning or auditory perception pathway have specialized into subregions that control the production of learned vocalizations (9–11).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [9] Feenders G Molecular mapping of movement-associated areas in the avian brain: A motor theory for vocal learning origin PLOS ONE 3 e1768 2008 10.1371/journal.pone.0001768 18335043 PMC2258151
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- cites [10] Margoliash D Distributed representation in the song system of oscines: Evolutionary implications and functional consequences Brain Behav Evol 44 247 264 1994 10.1159/000113580 7842284
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- cites [11] Mello CV Vates GE Okuhata S Nottebohm F Descending auditory pathways in the adult male zebra finch (Taeniopygia guttata) J Comp Neurol 395 137 160 1998 10.1002/(SICI)1096-9861(19980601)395:2<137::AID-CNE1>3.0.CO;2-3 9603369
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May combine two claims.
Premisenone givenThe vocal-learning circuits include a corticostriatal loop and a unique direct connection from motor cortical areas (human LMC and songbird RA) to brainstem vocal motor and respiratory neurons for phonation.
“These circuits include a corticostriatal loop and a unique direct connection from motor cortical areas [human laryngeal motor cortex (LMC) and songbird robust nucleus of the arcopallium (RA)] to brainstem vocal motor and respiratory neurons for phonation (Fig. 1).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Fig. 1
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PremisecitationFOXP2 transcription factor is required for vocal learning in both humans and songbirds, suggesting neural circuits for vocal learning across clades may have evolved overlapping molecular mechanisms.
“The FOXP2 transcription factor is required for vocal learning in both humans (20) and songbirds (21–24), which suggests that neural circuits for vocal learning across clades may have evolved overlapping molecular mechanisms.”
Quote in the paperSubstantial claim0 of 5 sources checked- cites [20] Lai CS Fisher SE Hurst JA Vargha-Khadem F Monaco AP A forkhead-domain gene is mutated in a severe speech and language disorder Nature 413 519 523 2001 10.1038/35097076 11586359
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- cites [21] Haesler S FoxP2 expression in avian vocal learners and non-learners J Neurosci 24 3164 3175 2004 10.1523/JNEUROSCI.4369-03.2004 15056696 PMC6730012
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- cites [22] Haesler S Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X PLOS Biol 5 e321 2007 10.1371/journal.pbio.0050321 18052609 PMC2100148
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- cites [23] Scharff C Petri J Evo-devo, deep homology and FoxP2: Implications for the evolution of speech and language Philos Trans R Soc London Ser B 366 2124 2140 2011 10.1098/rstb.2011.0001 21690130 PMC3130369
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- cites [24] Teramitsu I Kudo LC London SE Geschwind DH White SA Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction J Neurosci 24 3152 3163 2004 10.1523/JNEUROSCI.5589-03.2004 15056695 PMC6730014
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Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationSome glutamate receptors have specialized expression in forebrain song and speech areas in birds and humans, but a direct comparison between species was not made.
“Some glutamate receptors were found to have specialized expression in forebrain song and speech areas in birds (19) and humans (18), but a direct comparison between species was not made.”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [18] Amunts K Broca’s region: Novel organizational principles and multiple receptor mapping PLOS Biol 8 e1000489 2010 10.1371/journal.pbio.1000489 20877713 PMC2943440 source
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- cites [19] Wada K Sakaguchi H Jarvis ED Hagiwara M Differential expression of glutamate receptors in avian neural pathways for learned vocalization J Comp Neurol 476 44 64 2004 10.1002/cne.20201 15236466 PMC2517240
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Classified as probably not a substantial claim.
PremisecitationA potential mechanism for convergent evolution of brain systems is that a larger brain structure (superregion) specializes into multiple subregions, each performing a distinct function.
“A potential mechanism for convergent evolution of brain systems is one in which a larger brain structure (superregion) specializes into multiple subregions, each of which performs a distinct function (7–9).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [7] Oakley TH Rivera AS Genomics and the evolutionary origins of nervous system complexity Curr Opin Genet Dev 18 479 492 2008 10.1016/j.gde.2008.12.002 19152785
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- cites [8] Barrett HC A hierarchical model of the evolution of human brain specializations Proc Natl Acad Sci USA 109 suppl 1 10733 10740 2012 10.1073/pnas.1201898109 22723350 PMC3386868
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- cites [9] Feenders G Molecular mapping of movement-associated areas in the avian brain: A motor theory for vocal learning origin PLOS ONE 3 e1768 2008 10.1371/journal.pone.0001768 18335043 PMC2258151
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationFor echolocating mammals, genome-scale convergence in amino acid sequence was found in many genes involved in hearing.
“In addition, for echolocating mammals, genome-scale convergence in amino acid sequence was recently found in many genes involved in hearing (31).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [31] Parker J Genome-wide signatures of convergent evolution in echolocating mammals Nature 502 228 231 2013 10.1038/nature12511 24005325 PMC3836225
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May combine two claims.
Interpretationown dataThe authors did not find a strong correlation between avian striatal regions (Area X and VS) and human pallidum, supporting the conclusion that the avian regions are predominantly striatal.
“Although some avian striatal regions (Area X and VS) are known to have a sparse population of pallidum-like neurons (46–48), we did not find a strong correlation with the human pallidum (Table 1), supporting the conclusion that the avian regions are predominantly striatal (33, 44).”
Quote in the paperSubstantial claim0 of 5 sources checked- cites [46] Carrillo GD Doupe AJ Is the songbird Area X striatal, pallidal, or both? An anatomical study J Comp Neurol 473 415 437 2004 10.1002/cne.20099 15116398
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- cites [47] Reiner A Laverghetta AV Meade CA Cuthbertson SL Bottjer SW An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch J Comp Neurol 469 239 261 2004 10.1002/cne.11012 14694537
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- cites [48] Farries MA Perkel DJ A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus J Neurosci 22 3776 3787 2002 11978853 PMC6758399
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- cites [33] Zhang G Comparative genomics reveals insights into avian genome evolution and adaptation Science 346 1311 1320 2014 10.1126/science.1251385 25504712 PMC4390078
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- cites [44] Reiner A The Avian Brain Nomenclature Forum: Terminology for a new century in comparative neuroanatomy J Comp Neurol 473 E1 E6 2004 19626136 PMC2713747
Not checked in the free run.
- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationcitationThe lower significance for avian pallium-human cortex similarity could possibly reflect greater differences between avian pallium and human cortex than between avian and human striatum.
“The lower significance could possibly reflect greater differences between the avian pallium and human cortex than between the avian and human striatum (33, 47).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [33] Zhang G Comparative genomics reveals insights into avian genome evolution and adaptation Science 346 1311 1320 2014 10.1126/science.1251385 25504712 PMC4390078
Not checked in the free run.
- cites [47] Reiner A Laverghetta AV Meade CA Cuthbertson SL Bottjer SW An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch J Comp Neurol 469 239 261 2004 10.1002/cne.11012 14694537
Not checked in the free run.
- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Interpretationown dataThese results support the cortex hypothesis and contradict the claustrum-amygdala hypothesis of homologies between avian and mammalian pallial brain regions.
“These results support the cortex hypothesis (33, 43, 44) and contradict the claustrum-amygdala hypothesis of homologies between avian and mammalian pallial brain regions (33, 45).”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [33] Zhang G Comparative genomics reveals insights into avian genome evolution and adaptation Science 346 1311 1320 2014 10.1126/science.1251385 25504712 PMC4390078
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- cites [43] Jarvis ED Global view of the functional molecular organization of the avian cerebrum: Mirror images and functional columns J Comp Neurol 521 3614 3665 2013 23818122 PMC4145244
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- cites [44] Reiner A The Avian Brain Nomenclature Forum: Terminology for a new century in comparative neuroanatomy J Comp Neurol 473 E1 E6 2004 19626136 PMC2713747
Not checked in the free run.
- cites [45] Puelles L Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1 J Comp Neurol 424 409 438 2000 10.1002/1096-9861(20000828)424:3<409::AID-CNE3>3.0.CO;2-7 10906711
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- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Study design and conductcitationThe authors used only animals that did not sing after an overnight period of silence alone, because neural activity associated with singing causes changes in expression of thousands of genes in the song nuclei.
“We used only animals that did not sing after an overnight period of silence alone, because neural activity associated with singing causes changes in expression of thousands of genes in the song nuclei (37, 42).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [37] Whitney O Science 346 1256780 2014 10.1126/science.1256780 25504732 PMC4359888
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- cites [42] Jarvis ED Nottebohm F Motor-driven gene expression Proc Natl Acad Sci USA 94 4097 4102 1997 10.1073/pnas.94.8.4097 9108111 PMC20574
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Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationConvergent changes in amino acid sequence among vocal-learning birds and mammals have recently been reported.
“Likewise, convergent changes in amino acid sequence among vocal-learning birds and mammals have recently been reported (32, 33).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [32] Wang R thesis Duke University 2011 http://dukespace.lib.duke.edu/dspace/bitstream/handle/10161/5630/Wang_duke_0066D_10911.pdf?sequence=1
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- cites [33] Zhang G Comparative genomics reveals insights into avian genome evolution and adaptation Science 346 1311 1320 2014 10.1126/science.1251385 25504712 PMC4390078
Not checked in the free run.
May combine two claims.
PremisecitationSong-learning birds and humans are separated from a common ancestor by more than 68 million years among birds or 310 million years between birds and humans.
“We examined whether complex behavioral and anatomical convergence is associated with molecular convergence in song-learning birds and humans, species separated from a common ancestor by more than 68 million years (among birds) or 310 million years (between birds and humans) (34–36).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [34] Jarvis ED Avian brains and a new understanding of vertebrate brain evolution Nat Rev Neurosci 6 151 159 2005 10.1038/nrn1606 15685220 PMC2507884
Not checked in the free run.
- cites [35] Kumar S Hedges SB A molecular timescale for vertebrate evolution Nature 392 917 920 1998 10.1038/31927 9582070 source
Not checked in the free run.
- cites [36] Jarvis ED Whole-genome analyses resolve early branches in the tree of life of modern birds Science 346 1320 1331 2014 10.1126/science.1253451 25504713 PMC4405904 source
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May combine two claims.
PremisecitationSongbird RA and HVC are part of a vocal motor pathway that controls production of learned vocalizations, whereas Area X and LMAN are part of a pathway that controls imitation and exploration of vocalizations.
“The songbird RA and HVC are part of a vocal motor pathway that controls the production of learned vocalizations, whereas Area X and LMAN are part of a pathway that controls imitation and exploration of vocalizations (Fig. 1A) (40, 41).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [40] Brainard MS Doupe AJ Translating birdsong: Songbirds as a model for basic and applied medical research Annu Rev Neurosci 36 489 517 2013 10.1146/annurev-neuro-060909-152826 23750515 PMC4130661
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- cites [41] Jarvis ED Learned birdsong and the neurobiology of human language Ann NY Acad Sci 1016 749 777 2004 10.1196/annals.1298.038 15313804 PMC2485240
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Interpretationown dataAvian RA and arcopallium are similar to mammalian layer 5 cells, but each vocal-learning species' RA analog has greater similarity to human laryngeal cortex regions relative to nonhuman primate motor cortex.
“These findings demonstrate the similarity of avian RA and arcopallium to mammalian layer 5 cells, but a greater similarity of each vocal-learning species’ RA analog to human laryngeal cortex regions (which also contain layer 5 cells) relative to nonhuman primate motor cortex.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationcitationThe similarity to somatosensory cortex is not too surprising, considering the underappreciated overlap of cells with motor and somatosensory functions in both walls of the central sulcus.
“The similarity to the somatosensory cortex is not too surprising, considering the underappreciated overlap of cells with motor and somatosensory functions in both walls (PrG_cs and PoG_cs) of the central sulcus (55).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [55] Nii Y Uematsu S Lesser RP Gordon B Does the central sulcus divide motor and sensory functions? Cortical mapping of human hand areas as revealed by electrical stimulation through subdural grid electrodes Neurology 46 360 367 1996 10.1212/WNL.46.2.360 8614495
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- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
May combine two claims.
Interpretationown dataThe similarity between RA and the broader primary motor cortex in humans is due in part to similarity with its layer 5 neurons, and is separate from the similarities to LMC/dLSC within primary motor cortex.
“These findings indicate that the similarity between RA and the broader primary motor cortex in humans is due in part to similarity with its layer 5 neurons, and is separate from the similarities to LMC/dLSC within primary motor cortex.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
Probably not a substantial claim: may not pass S2 (checkable).
InterpretationreasoningThe genes and their expression differences can serve as candidates that can lead us to the cause.
“the genes and their expression differences can serve as candidates that can lead us to the cause”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationConvergent gene expression for RA/LMC and Area X/putamen involves species separated from a common ancestor by 68 million to 310 million years, different vertebrate lineages, and many genes.
“We find the convergent gene expression for RA/LMC and Area X/putamen remarkable in that they involve species separated from a common ancestor by 68 million to 310 million years (34–36), different vertebrate lineages, and many genes.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [34] Jarvis ED Avian brains and a new understanding of vertebrate brain evolution Nat Rev Neurosci 6 151 159 2005 10.1038/nrn1606 15685220 PMC2507884
Not checked in the free run.
- cites [35] Kumar S Hedges SB A molecular timescale for vertebrate evolution Nature 392 917 920 1998 10.1038/31927 9582070 source
Not checked in the free run.
- cites [36] Jarvis ED Whole-genome analyses resolve early branches in the tree of life of modern birds Science 346 1320 1331 2014 10.1126/science.1253451 25504713 PMC4405904 source
Not checked in the free run.
May combine two claims.
InterpretationreasoningOur analyses do not show that the specializations discovered are functionally related to the projections of these neurons or to vocal learning.
“our analyses do not show that the specializations we discovered are functionally related to the projections of these neurons or to vocal learning”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataThe correlations are highly significant and predominantly driven by specialized expression of tens to hundreds of genes out of thousands, and for vocal-learning regions are supported by lack of such findings in vocal-nonlearning birds and primates.
“Although the correlations we find at first glance may not seem strong, they are highly significant, are predominantly driven by the specialized expression of tens to hundreds of genes (depending on the level in the anatomical tree) out of thousands of genes, and for vocal-learning regions are supported by lack of such findings in vocal-nonlearning birds and primates.”
Quote in the paperSubstantial claimMay combine two claims.
InterpretationreasoningThe match of Area X to human striatum and RA analogs to cortex enables specific hypotheses about which brain regions are analogous in song-learning birds and humans, and which regions in humans may be specialized for speech.
“The match of Area X to the human striatum and of RA analogs to the cortex enables specific hypotheses about which brain regions are analogous in song-learning birds and humans, as well as which regions in humans may be specialized for speech.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationROBO1 mutations cause dyslexia and speech disorders in humans.
“ROBO1 mutations cause dyslexia and speech disorders in humans (76)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [76] Fisher SE Francks C Genes, cognition and dyslexia: Learning to read the genome Trends Cognit Sci 10 250 257 2006 10.1016/j.tics.2006.04.003 16675285
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Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationThe role of human striatum in speech acquisition and production has begun to be appreciated, but specific loci have not been as well defined as for cortex.
“The role of the human striatum in speech acquisition and production has begun to be appreciated (57, 83), but specific loci have not been as well defined as for the cortex.”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [57] Brown S The somatotopy of speech: Phonation and articulation in the human motor cortex Brain Cognit 70 31 41 2009 10.1016/j.bandc.2008.12.006 19162389 PMC2873785 source
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- cites [83] Simonyan K Horwitz B Jarvis ED Dopamine regulation of human speech and bird song: A critical review Brain Lang 122 142 150 2012 10.1016/j.bandl.2011.12.009 22284300 PMC3362661
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May combine two claims.
PremisecitationParvalbumin is present at unusually high levels in RA neurons that project to vocal motor neurons in songbirds and in analogous layer 5 neurons of oral motor cortex of humans and chimpanzees, but not in projection neurons of adjacent arcopallium or in oral motor cortex of other primates or mammals.
“the calcium-buffering protein parvalbumin has been noted (16) to be present at unusually high levels in the RA neurons that project to vocal motor neurons in songbirds and in the analogous layer 5 neurons of oral motor cortex (containing vLMC) of humans and chimpanzees, but not in the projection neurons of the adjacent arcopallium or in the oral motor cortex of other primates or mammals (79, 80).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [16] Hara E Rivas MV Ward JM Okanoya K Jarvis ED Convergent differential regulation of parvalbumin in the brains of vocal learners PLOS ONE 7 e29457 2012 10.1371/journal.pone.0029457 22238614 PMC3253077
Not checked in the free run.
- cites [79] Wild JM Williams MN Suthers RA Parvalbumin-positive projection neurons characterise the vocal premotor pathway in male, but not female, zebra finches Brain Res 917 235 252 2001 10.1016/S0006-8993(01)02938-9 11640910
Not checked in the free run.
- cites [80] Sherwood CC Holloway RL Erwin JM Hof PR Cortical orofacial motor representation in Old World monkeys, great apes, and humans. II. Stereologic analysis of chemoarchitecture Brain Behav Evol 63 82 106 2004 10.1159/000075673 14685003
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationdLMC was only recently described.
“the dLMC was also only recently described (63)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [63] Brown S Ngan E Liotti M A larynx area in the human motor cortex Cereb Cortex 18 837 845 2008 10.1093/cercor/bhm131 17652461 source
Not checked in the free run.
Classified as probably not a substantial claim.
PremisecitationA recent study argued avian pallium is equally and only weakly similar to mouse cortex, claustrum, or amygdala.
“a recent study that used brain transcriptome profiles to argue that the avian pallium is equally and only weakly similar to the mouse cortex, claustrum, or amygdala (68)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [68] Belgard TG Adult pallium transcriptomes surprise in not reflecting predicted homologies across diverse chicken and mouse pallial sectors Proc Natl Acad Sci USA 110 13150 13155 2013 10.1073/pnas.1307444110 23878249 PMC3740902
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningThis lack does not mean that shared specializations of more specific regions within cortex do not exist.
“does not mean that shared specializations of more specific regions within the cortex do not exist”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataOur ability to identify a stronger relationship to cortex was because we organized expression profiles as specialization trees, developed a dynamic programming algorithm requiring hierarchical anatomical alignment of brain similarities, and performed avian brain dissections using more precise laser capture microdissections.
“We believe our ability to identify a stronger relationship to the cortex was because we organized the expression profiles as specialization trees, developed a dynamic programming algorithm requiring hierarchical anatomical alignment of brain similarities, and performed avian brain dissections using more precise laser capture microdissections.”
Quote in the paperSubstantial claim
The authors state this as an assumption.
The human premortem vocalizing state is unknown, but it is assumed not to prevent identification of convergent gene expression specializations as long as one species was silent, the genes are not sensitive to immediate vocalizing behavior, and human samples were collected 10 to 30 hours postmortem when many vocalizing-regulated gene expression changes have subsided.
“We do not know the premortem vocalizing state of the humans, but did not expect this to prevent us from identifying convergent gene expression specializations as long as one species was silent (the birds), the genes are not sensitive to immediate vocalizing behavior, and the human samples were collected 10 to 30 hours postmortem, when many of the vocalizing-regulated gene expression changes have”
The paper relies on this without support.
No examples of widespread convergence in gene expression patterns in brain regions involved in convergently evolved behavioral traits were known before this study.
“However, we are not aware of examples of widespread convergence in gene expression patterns in brain regions involved in convergently evolved behavioral traits.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Studies on avian vocal learners have shown a convergent differential regulation of axon guidance genes of the SLIT-ROBO families in the pallial motor nucleus of the learning species, allowing for the formation of connections virtually absent in the brains of vocal non-learners.
“Studies conducted on avian vocal learners89,90 have shown a convergent differential regulation of axon guidance genes of the SLIT-ROBO families in the pallial motor nucleus of the learning species, allowing for the formation of connections virtually absent in the brains of vocal non-learners.”
From A catalog of single nucleotide changes distinguishing modern humans from archaic hominins (2019) · cites this paper as [89]
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Core and region-enriched networks of behaviorally regulated genes and the singing genome
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Self-citationReiner, A. J., Laverghetta, A., Meade, C. A., Cuthbertson, S. L., & Bottjer, S. W. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.11012 · Cited by 110 · see citing works
Birdsong “Transcriptomics”: Neurochemical Specializations of the Oscine Song System
Lovell, P. V., Clayton, D. F., Replogle, K. L., & Mello, C. V. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003440 · Cited by 102 · cited 1× · see citing works
“We attempted to analyze an available data set of HVC and the surrounding auditory nidopallium shelf, generated with cDNA microarrays (12).”
Self-citationMargoliash, D., Fortune, E., Sutter, M. L., Yu, A. C., Wren-Hardin, B. D., & Dave, A. (1994) · Brain, Behavior and Evolution · doi:10.1159/000113580 · Cited by 98 · see citing works
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Self-citationIs the songbird Area X striatal, pallidal, or both? an anatomical study
Carrillo, G. D., & Doupe, A. J. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20099 · Cited by 92 · see citing works
Chen, C.-C., Winkler, C. M., Pfenning, A., & Jarvis, E. D. (2013) · The Journal of comparative neurology · doi:10.1002/cne.23406 · Cited by 88 · see citing works
Self-citationDopamine regulation of human speech and bird song: A critical review
Simonyan, K., Horwitz, B., & Jarvis, E. D. (2012) · Brain and Language · doi:10.1016/j.bandl.2011.12.009 · Cited by 84 · cited 1× · see citing works
“The role of the human striatum in speech acquisition and production has begun to be appreciated (57, 83), but specific loci have not been as well defined as for the cortex.”
Self-citationBelgard, T. G., Montiel, J. F., Wang, W. Z., García‐Moreno, F., Margulies, E. H., Ponting, C. P., & Molnár, Z. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307444110 · Cited by 82 · see citing works
High-coverage sequencing and annotated assemblies of the budgerigar genome
Ganapathy, G., Howard, J. T., Ward, J. M., Li, J., Li, B., Li, Y., Xiong, Y., Zhang, Y., Zhou, S., Schwartz, D. C., et al. (2014) · GigaScience · doi:10.1186/2047-217x-3-11 · Cited by 81 · see citing works
Self-citationConvergent differential regulation of SLIT-ROBO axon guidance genes in the brains of vocal learners
Wang, R., Chen, C., Hara, E., Rivas, M. V., Roulhac, P. L., Howard, J. T., Chakraborty, M., Audet, J., & Jarvis, E. D. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23719 · Cited by 74 · see citing works
Self-citationParallel FoxP1 and FoxP2 Expression in Songbird and Human Brain Predicts Functional Interaction
Teramitsu, I., Kudo, L., London, S. E., Geschwind, D., & White, S. A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5589-03.2004 · Cited by 64 · see citing works
Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans
Sherwood, C. C., Holloway, R. L., ERWIN, J. M., & Hof, P. R. (2003) · Brain Behavior and Evolution · doi:10.1159/000075673 · Cited by 62 · cited 1× · see citing works
“Among the very few genes with convergent up-regulation in RA and LMC, the calciumbuffering protein parvalbumin has been noted (16) to be present at unusually high levels in the RA neurons that project to vocal motor neurons in songbirds and in the analogous layer 5 neurons of oral motor cortex (containing vLMC) of hum…”
Cell-type–based model explaining coexpression patterns of genes in the brain
Grange, P., Bohland, J. W., Okaty, B. W., Sugino, K., Bokil, H., Nelson, S. B., Ng, L., Hawrylycz, M., & Mitra, P. P. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312098111 · Cited by 61 · see citing works
Li, X.-C., Wang, X., Tannenhauser, J., Podell, S. B., Mukherjee, P., Hertel, M., Biane, J. S., Masuda, S., Nottebohm, F., & Gaasterland, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701619104 · Cited by 58 · see citing works
Horita, H., Kobayashi, M., Liu, W.-C., Oka, K., Jarvis, E., & Wada, K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042173 · Cited by 53 · see citing works
Self-citationConvergent Differential Regulation of Parvalbumin in the Brains of Vocal Learners
Hara, E., Rivas, M., Ward, J. M., Okanoya, K., & Jarvis, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029457 · Cited by 53 · cited 6× · see citing works
“We leveraged the expression profiles of thousands of genes that we (supplementary materials section SM1) and others collected from the brains of vocal-learning and vocal-nonlearning birds (15, 16, 37), humans (http://human.”
InfluentialSelf-citationThe Avian Brain Nomenclature Forum: Terminology for a New Century in Comparative Neuroanatomy.
Reiner, A. J., Perkel, D. J., Bruce, L. L., Butler, A. B., Csillag, A., Kuenzel, W. J., Medina, L. M., Paxinos, G., Shimizu, T., Striedter, G. F., et al. (2004) · PubMed · doi:10.1002/cne.20119 · Cited by 50 · cited 10× · see citing works
“Striatum to Area X Striatum to putamen (41, 44) 0.”
InfluentialSelf-citationWild, J. M., Williams, M. N., & Suthers, R. A. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02938-9 · Cited by 46 · see citing works
Dlx6 regulates molecular properties of the striatum and central nucleus of the amygdala
Wang, B., Lufkin, T., & Rubenstein, J. L. R. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22618 · Cited by 44 · see citing works
Lovell, P. V., Carleton, J. B., & Mello, C. V. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-470 · Cited by 40 · see citing works
Self-citationA framework for integrating the songbird brain
Jarvis, E., Smith, V. A., Wada, K., Rivas, M. V., McElroy, M. B., Smulders, T. V., Carninci, P., Hayashizaki, Y., Dietrich, F., Wu, X., et al. (2002) · Journal of Comparative Physiology A · doi:10.1007/s00359-002-0358-y · Cited by 39 · see citing works
Self-citationAdret, P., & Margoliash, D. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10459 · Cited by 35 · cited 1× · see citing works
“This is supported by the fact that the RA neurons have a higher spontaneous firing rate than the surrounding arcopallium (81).”
Neural Substrates for String-Context Mutual Segmentation: A Path to Human Language
Okanoya, K., & Merker, B. H. (2007) · Springer eBooks · doi:10.1007/978-1-84628-779-4_22 · Cited by 35 · see citing works
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Self-citationMicroproteomics: Quantitative Proteomic Profiling of Small Numbers of Laser-Captured CellsPreprint
Roulhac, P. L., Ward, J. M., Thompson, J. W., Soderblom, E. J., Silva, M., Moseley, M. A., & Jarvis, E. D. (2011) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5573 · Cited by 34 · see citing works
Self-citationAn Optimized Protocol for High-Throughput In Situ Hybridization of Zebra Finch BrainPreprint
Carleton, J. B., Lovell, P. V., McHugh, A. K., Marzulla, T., Horback, K. L., & Mello, C. V. (2014) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot084582 · Cited by 32 · see citing works
Self-citationDynamics of crowing development in the domestic Japanese quail (Coturnix coturnix japonica)
Derégnaucourt, S., Saar, S., & Gahr, M. L. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.0016 · Cited by 32 · cited 1× · see citing works
“We first looked for possible specializations in the gene expression profiles of the RA analog from species representing the two other vocal-learning lineages (parrots and hummingbirds) compared to the neighboring arcopallium and comparably located regions of the arcopallium of species representing two experimentally d…”
Imaging features of multicentric Castleman's disease in HIV infection
Hillier, J. C., Shaw, P. J., Miller, R. F., Cartledge, J. D., Nelson, M. R., Bower, M., Francis, N. A., & Padley, S. P. G. (2004) · Clinical Radiology · doi:10.1016/j.crad.2003.10.025 · Cited by 32 · see citing works
Striatum specific protein, Rhes regulates AKT pathway
Bang, S., Steenstra, C., & Kim, S. F. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.05.073 · Cited by 29 · see citing works
Molecular characterization of the song control nucleus HVC in Bengalese finch brain
Kato, M., & Okanoya, K. (2010) · Brain Research · doi:10.1016/j.brainres.2010.09.014 · Cited by 28 · see citing works
Self-citationHilliard, A. T., Miller, J. E., Horvath, S., & White, S. A. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002773 · Cited by 27 · see citing works
Genomics and the evolutionary origins of nervous system complexity
Oakley, T. H., & Rivera, A. S. (2008) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.12.002 · Cited by 26 · see citing works
Dubbeldam, J. L. (1998) · Cells Tissues Organs · doi:10.1159/000046494 · Cited by 24 · see citing works
Radioactive in situ Hybridization for Detecting Diverse Gene Expression Patterns in Tissue
Chen, C., Wada, K., & Jarvis, E. D. (2012) · Journal of Visualized Experiments · doi:10.3791/3764 · Cited by 21 · see citing works
Self-citationRole of Slit and Robo Proteins in the Development of Dopaminergic Neurons
Cornide‐Petronio, M. E., & Barreiro‐Iglesias, A. (2013) · Developmental Neuroscience · doi:10.1159/000351023 · Cited by 20 · cited 1× · see citing works
“Thus, because binding of SLIT1 to ROBO1 causes repulsion of the axonal processes from cell bodies (78), we hypothesize that the down-regulation of SLIT1 and other neural connectivity genes in RA and LMC may represent a permissive mechanism to allow certain neural connections to form, such as the unique direct projecti…”
Matsunaga, E., Suzuki, K., Kobayashi, T., & Okanoya, K. (2011) · Development, Growth and Differentiation · doi:10.1111/j.1440-169x.2011.01302.x · Cited by 16 · see citing works
Clayton, D. F., George, J. M., Mello, C. V., & Siepka, S. M. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20686 · Cited by 14 · see citing works
Self-citationSasaki, T., Komatsu, Y., Watakabe, A., Sawada, K., & Yamamori, T. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp319 · Cited by 13 · cited 1× · see citing works
“Likewise, macaques have recently been shown to have lower SLIT1 in primary motor cortex (69), which we also found in marmosets (fig.”
Correction: A role for descending auditory cortical projections in songbird vocal learning
Mandelblat-Cerf, Y., Las, L., Denisenko-Nehrbass, N., & Fee, M. S. (2014) · eLife · doi:10.7554/elife.04371 · Cited by 11 · see citing works
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Towards complete and error-free genome assemblies of all vertebrate species
Rhie, A., McCarthy, S. A., Fedrigo, O., Damas, J., Formenti, G., Koren, S., Uliano-Silva, M., Chow, W., Fungtammasan, A., Kim, J., et al. (2021) · Nature · doi:10.1038/s41586-021-03451-0 · Cited by 3,097 · see citing works
Self-citationComparative genomics reveals insights into avian genome evolution and adaptation
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Self-citationBirds have primate-like numbers of neurons in the forebrain
Olkowicz, S., Kocourek, M., Lučan, R. K., Porteš, M., Fitch, W. T., Herculano-Houzel, S., & Němec, P. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1517131113 · Cited by 564 · see citing works
Güntürkün, O., & Bugnyar, T. (2016) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.02.001 · Cited by 388 · see citing works
The origin and diversification of birds
Brusatte, S. L., O’Connor, J. K., & Jarvis, E. D. (2015) · Current Biology · doi:10.1016/j.cub.2015.08.003 · Cited by 334 · see citing works
Self-citationEvolution of vocal learning and spoken language
Jarvis, E. (2019) · Science · doi:10.1126/science.aax0287 · Cited by 249 · see citing works
Self-citationEvolutionary constraint and innovation across hundreds of placental mammals
Christmas, M. J., Kaplow, I. M., Genereux, D. P., Dong, M. X., Hughes, G. M., Li, X., Sullivan, P. F., Hindle, A. G., Andrews, G., Armstrong, J. C., et al. (2023) · Science · doi:10.1126/science.abn3943 · Cited by 257 · see citing works
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Self-citationTeeling, E. C., Vernes, S. C., Dávalos, L. M., Ray, D. A., Gilbert, M. T. P., & Myers, E. W. (2017) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-022516-022811 · Cited by 233 · see citing works
Self-citationUnderstanding Human Cognitive Uniqueness
Laland, K. N., & Seed, A. M. (2021) · Annual Review of Psychology · doi:10.1146/annurev-psych-062220-051256 · Cited by 205 · see citing works
The Control of Vocal Pitch in Human Laryngeal Motor Cortex
Dichter, B. K., Breshears, J. D., Leonard, M. K., & Chang, E. F. (2018) · Cell · doi:10.1016/j.cell.2018.05.016 · Cited by 183 · see citing works
Yang, X., Hu, R., Yin, H., Jenkins, J. W., Shu, S., Tang, H., Liu, D., Weighill, D. A., Yim, W. C., Ha, J., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01491-7 · Cited by 198 · see citing works
Symbols and mental programs: a hypothesis about human singularity
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Neuronal factors determining high intelligence
Dicke, U., & Roth, G. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0180 · Cited by 175 · see citing works
Towards complete and error-free genome assemblies of all vertebrate species
Rhie, A., McCarthy, S. A., Fedrigo, O., Damas, J., Formenti, G., Koren, S., Uliano-Silva, M., Chow, W., Fungtammasan, A., Gedman, G. L., et al. (2020) · doi:10.1101/2020.05.22.110833 · Cited by 3,097 · see citing works
Self-citationCellular transcriptomics reveals evolutionary identities of songbird vocal circuits
Colquitt, B. M., Merullo, D. P., Konopka, G., Roberts, T. F., & Brainard, M. S. (2021) · Science · doi:10.1126/science.abd9704 · Cited by 169 · see citing works
Molecular and network-level mechanisms explaining individual differences in autism spectrum disorder
Buch, A. M., Vértes, P. E., Seidlitz, J., Kim, S. H., Grosenick, L., & Liston, C. M. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01259-x · Cited by 156 · see citing works
The origins of the vocal brain in humans
Belyk, M., & Brown, S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.014 · Cited by 144 · see citing works
The wild species genome ancestry of domestic chickens
Lawal, R. A., Martin, S. H., Vanmechelen, K., Vereijken, A., Silva, P., Al-Atiyat, R. M., Aljumaah, R. S., Mwacharo, J. M., Wu, D., Zhang, Y., et al. (2020) · BMC Biology · doi:10.1186/s12915-020-0738-1 · Cited by 158 · see citing works
Brain evolution by brain pathway duplication
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Self-citationUnderstanding Language from a Genomic Perspective
Graham, S. A., & Fisher, S. E. (2015) · Annual Review of Genetics · doi:10.1146/annurev-genet-120213-092236 · Cited by 135 · see citing works
Vertebrate brains and evolutionary connectomics: on the origins of the mammalian ‘neocortex’
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Beyond brain size: Uncovering the neural correlates of behavioral and cognitive specialization
Logan, C., Avin, S., Boogert, N. J., Buskell, A., Cross, F. R., Currie, A., Jelbert, S. A., Lukas, D., Marés, R., Navarrete, A. F., et al. (2018) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2018.130008 · Cited by 120 · see citing works
The Forebrain Song System Mediates Predictive Call Timing in Female and Male Zebra Finches
Benichov, J. I., Benezra, S. E., Vallentin, D., Globerson, E., Long, M. A., & Tchernichovski, O. (2016) · Current Biology · doi:10.1016/j.cub.2015.12.037 · Cited by 121 · see citing works
The functions of vocal learning in parrots
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Core and region-enriched networks of behaviorally regulated genes and the singing genome
Whitney, O., Pfenning, A. R., Howard, J. T., Blatti, C. A., Liu, F., Ward, J. M., Wang, R., Audet, J., Kellis, M., Mukherjee, S., et al. (2014) · Science · doi:10.1126/science.1256780 · Cited by 115 · see citing works
Self-citationConserved transcriptomic profiles underpin monogamy across vertebrates
Young, R. L., Ferkin, M. H., Ockendon-Powell, N., Orr, V. N., Phelps, S. M., Pogány, Á., Richards‐Zawacki, C. L., Summers, K., Székely, T., Trainor, B. C., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1813775116 · Cited by 114 · see citing works
A catalog of single nucleotide changes distinguishing modern humans from archaic hominins
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Blaxter, M., Archibald, J. M., Childers, A. K., Coddington, J. A., Crandall, K. A., Palma, F. D., Durbin, R. M., Edwards, S. V., Graves, J. A. M., Hackett, K. J., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2115636118 · Cited by 104 · see citing works
Self-citationThe Biology and Evolution of Speech: A Comparative Analysis
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Rhythmic Continuous-Time Coding in the Songbird Analog of Vocal Motor Cortex
Lynch, G. F., Okubo, T. S., Hanuschkin, A., Hahnloser, R. H. R., & Fee, M. S. (2016) · Neuron · doi:10.1016/j.neuron.2016.04.021 · Cited by 102 · see citing works
Chabout, J., Sarkar, A., Patel, S. R., Radden, T., Dunson, D. B., Fisher, S. E., & Jarvis, E. D. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00197 · Cited by 101 · see citing works
Self-citationLanguage Evolution: A Changing Perspective
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Lombardo, M. V., Pramparo, T., Gazestani, V., Warrier, V., Bethlehem, R. A. I., Barnes, C. C., Lopez, L., Lewis, N. E., Eyler, L. T., Pierce, K., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0281-3 · Cited by 95 · see citing works
Karyotype Evolution in Birds: From Conventional Staining to Chromosome Painting
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Convergent evolution of complex brains and high intelligence
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Relating enhancer genetic variation across mammals to complex phenotypes using machine learning
Kaplow, I. M., Lawler, A. J., Schäffer, D. E., Srinivasan, C., Sestili, H. H., Wirthlin, M. E., Phan, B. N., Prasad, K., Brown, A. R., Zhang, X., et al. (2023) · Science · doi:10.1126/science.abm7993 · Cited by 90 · see citing works
Self-citationDevelopmental and genetic mechanisms of neural circuit evolution
Tosches, M. A. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.06.016 · Cited by 91 · see citing works
Parrot Genomes and the Evolution of Heightened Longevity and Cognition
Wirthlin, M. E., Lima, N. C. B., Guedes, R. L. M., Soares, A. E. R., de Almeida, L. G. P., Cavaleiro, N. P., de Morais, G. L., Chaves, A. V., Howard, J. T., Teixeira, M. D. M., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.10.050 · Cited by 89 · see citing works
Self-citationMapping Human Laryngeal Motor Cortex during Vocalization
Eichert, N., Papp, D., Mars, R. B., & Watkins, K. E. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa182 · Cited by 89 · see citing works
Herold, C., Coppola, V. J., & Bingman, V. P. (2015) · Hippocampus · doi:10.1002/hipo.22463 · Cited by 84 · see citing works
Metabolomics-based screening of salivary biomarkers for early diagnosis of Alzheimer's disease
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From sauropsids to mammals and back: New approaches to comparative cortical development
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What Have We Learned from the First 500 Avian Genomes?
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Convergent differential regulation of SLIT-ROBO axon guidance genes in the brains of vocal learners
Wang, R., Chen, C., Hara, E., Rivas, M. V., Roulhac, P. L., Howard, J. T., Chakraborty, M., Audet, J., & Jarvis, E. D. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23719 · Cited by 74 · see citing works
Self-citationCore and shell song systems unique to the parrot brain
Chakraborty, M., Walløe, S., Nedergaard, S., Fridel, E. E., Dabelsteen, T., Pakkenberg, B., Bertelsen, M. F., Dorrestein, G. M., Brauth, S. E., Durand, S. E., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0118496 · Cited by 86 · see citing works
Self-citationThe brain dynamics of linguistic computation
Murphy, E. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01515 · Cited by 79 · see citing works
A Modular Approach to Vocal Learning: Disentangling the Diversity of a Complex Behavioral Trait
Wirthlin, M. E., Chang, E., Knörnschild, M., Krubitzer, L., Mello, C., Miller, C., Pfenning, A., Vernes, S., Tchernichovski, O., & Yartsev, M. M. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.036 · Cited by 58 · see citing works
Self-citationFalse gene and chromosome losses in genome assemblies caused by GC content variation and repeats
Kim, J., Lee, C., Ko, B. J., Yoo, D. A., Won, S., Phillippy, A. M., Fedrigo, O. D., Zhang, G., Howe, K., Wood, J. M. D., et al. (2022) · Genome biology · doi:10.1186/s13059-022-02765-0 · Cited by 71 · see citing works
Self-citationResolving a phylogenetic hypothesis for parrots: implications from systematics to conservation
Provost, K. L., Joseph, L., & Smith, B. T. (2017) · Emu - Austral Ornithology · doi:10.1080/01584197.2017.1387030 · Cited by 72 · see citing works
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A hypothesis on a role of oxytocin in the social mechanisms of speech and vocal learning
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Self-citationMolecular networks of the FOXP2 transcription factor in the brain
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What bats have to say about speech and language
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Levels of Homology and the Problem of Neocortex
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The effect of listening to music on human transcriptome
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Duetting as a Collective Behavior
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The effect of music performance on the transcriptome of professional musicians
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Possible functional links among brain- and skull-related genes selected in modern humans
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The Neural Basis of Vocal Pitch Imitation in Humans
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The Molecular Basis of Human Brain Evolution
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Vocal learning: a language-relevant trait in need of a broad cross-species approach
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Developmental origins and evolution of pallial cell types and structures in birds
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High-throughput metabolomics enables biomarker discovery in prostate cancer
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Avian genomics: fledging into the wild!
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Birdsong Learning and Culture: Analogies with Human Spoken Language
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Self-citationNeural Representations Observed
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Music-listening regulates human microRNA expression
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What animals can teach us about human language: the phonological continuity hypothesis
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Auditory representation of learned sound sequences in motor regions of the macaque brain
Archakov, D., DeWitt, I., Kuśmierek, P., Ortiz-Rios, M., Cameron, D. J., Cui, D., Morin, E. L., VanMeter, J. W., Sams, M. E., Jääskeläinen, I. P., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1915610117 · Cited by 50 · see citing works
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Self-citationSound sequences in birdsong: how much do birds really care?
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The FOXP2-Driven Network in Developmental Disorders and Neurodegeneration
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Animal Models of Speech and Vocal Communication Deficits Associated With Psychiatric Disorders
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What can animal communication teach us about human language?
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Evolutionary Divergence of Gene and Protein Expression in the Brains of Humans and Chimpanzees
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Sex differences and rapid estrogen signaling: A look at songbird audition
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Genetic Mechanisms Underlying the Evolution of Connectivity in the Human Cortex
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“These neural pathways are either absent in vocal nonlearning species or rudimentary in many species according to a continuum hypothesis of vocal learning (Wild et al. 1997; Arriaga et al. 2012; Petkov and Jarvis 2012; Liu et al. 2013; Pfenning et al. 2014; Jarvis 2019).”
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The social role of song in wild zebra finches
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- Authors
- Pfenning, A. R., Hara, E., Whitney, O., Rivas, M. V., Wang, R., Roulhac, P. L., Howard, J. T., Wirthlin, M., Lovell, P. V., Ganapathy, G., Mountcastle, J., Moseley, M. A., Thompson, J. W., Soderblom, E. J., Iriki, A., Kato, M., Gilbert, M. T. P., Zhang, G., Bakken, T., Bongaarts, A., Bernard, A., Lein, E., Mello, C. V., Hartemink, A. J., & Jarvis, E. D.
- Affiliations
- Howard Hughes Medical Institute (US)
- Oregon Health & Science University (US)
- Duke University (US)
- RIKEN Center for Brain Science (JP)
- University of Copenhagen (DK)
- Allen Institute for Brain Science (US)
- Allen Institute for Brain Science, Seattle, WA 98103, USA.
- Corresponding author
- Pfenning, Andreas R.
- Hartemink, Alexander J.
- Jarvis, Erich D.
- ORCID
- Pfenning, Andreas R.
- Hara, Erina
- Whitney, Osceola
- Rivas, Miriam V.
- Howard, Jason T.
- Wirthlin, Morgan
- Lovell, Peter V.
- Mountcastle, Jacquelyn
- Moseley, M. Arthur
- Thompson, J. Will
- Soderblom, Erik J.
- Iriki, Atsushi
- Kato, Masaki
- Gilbert, M. Thomas P.
- Zhang, Guojie
- Bakken, Trygve
- Bernard, Amy
- Lein, Ed
- Mello, Claudio V.
- Hartemink, Alexander J.
- Jarvis, Erich D.
- Venue
- Science
- Published
- 2014-12-12
- Volume
- 346
- Issue
- 6215
- Pages
- 1256846-1256846
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC4385736
- OpenAlex
- W2052801529
- Semantic Scholar
- ff584b8778ab8ff5d15336d922fff27c76b7fb58
- Cited by
- 463
- References
- 117
- Citations by year
- 2026: 25 · 2025: 40 · 2024: 24 · 2023: 32 · 2022: 36 · 2021: 47 · 2020: 39 · 2019: 38 · 2018: 43 · 2017: 57 · 2016: 33 · 2015: 44 · 2014: 4 · 2013: 1
- FWCI
- 42.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
- eSpace (Curtin University) (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (DP1OD000448)
- National Institute on Deafness and Other Communication Disorders (R21DC007478, R01DC007218)
- National Institute of General Medical Sciences (R24GM092842)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Social Sciences › Cultural Studies › Language and cultural evolution
- Keywords
- vocal learning, human speech, convergent evolution, brain transcriptome, gene expression, song nuclei, striatum, motor control, brain connectivity, avian vocal learning
- MeSH terms
- Adult, Animals, Birds, Brain, Brain Mapping, Corpus Striatum, Gene Expression Regulation, Humans, Learning, Male, Motor Cortex, Neural Pathways, Species Specificity, Speech, Transcription, Genetic, Vocalization, Animal, Evolution, Molecular, Finches, Transcriptome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.
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