Convergent differential regulation of SLIT-ROBO axon guidance genes in the brains of vocal learners
Open accessAbstract
Only a few distantly related mammals and birds have the trait of complex vocal learning, which is the ability to imitate novel sounds. This ability is critical for speech acquisition and production in humans, and is attributed to specialized forebrain vocal control circuits that have several unique connections relative to adjacent brain circuits. As a result, it has been hypothesized that there could exist convergent changes in genes involved in neural connectivity of vocal learning circuits. In support of this hypothesis, expanding on our related study (Pfenning et al. [2014] Science 346: 1256846), here we show that the forebrain part of this circuit that makes a relatively rare direct connection to brainstem vocal motor neurons in independent lineages of vocal learning birds (songbird, parrot, and hummingbird) has specialized regulation of axon guidance genes from the SLIT-ROBO molecular pathway. The SLIT1 ligand was differentially downregulated in the motor song output nucleus that makes the direct projection, whereas its receptor ROBO1 was developmentally upregulated during critical periods for vocal learning. Vocal nonlearning bird species and male mice, which have much more limited vocal plasticity and associated circuits, did not show comparable specialized regulation of SLIT-ROBO genes in their nonvocal motor cortical regions. These findings are consistent with SLIT and ROBO gene dysfunctions associated with autism, dyslexia, and speech sound language disorders and suggest that convergent evolution of vocal learning was associated with convergent changes in the SLIT-ROBO axon guidance pathway.
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The Slit/Robo pathway has been proposed to be involved in vocal learning.
“the proposed involvement of this pathway in vocal learning [104, 105]”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [104]
FOXP2, ROBO1, and ROBO2 have long been implicated in brain wiring processes critical for vocal learning in several species, including humans.
“Among the genes downstream of BAZ1B that we uncovered in this study, FOXP2, ROBO1, and ROBO2 have long been implicated in brain wiring processes critical for vocal learning in several species (50, 51), including humans”
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 [90]
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)”
From Convergent transcriptional specializations in the brains of humans and song-learning birds (2014) · cites this paper as [70]
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).”
From Convergent transcriptional specializations in the brains of humans and song-learning birds (2014) · cites this paper as [70]
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”
From Convergent transcriptional specializations in the brains of humans and song-learning birds (2014) · cites this paper as [70]
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).”
From Convergent transcriptional specializations in the brains of humans and song-learning birds (2014) · cites this paper as [70]
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).”
From Convergent transcriptional specializations in the brains of humans and song-learning birds (2014) · cites this paper as [70]
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“the molecular diversification of axon guidance genes, thereby increasing crosstalk between different ligands and receptors (Dascenco et al., 2015; Delloye-Bourgeois et al., 2014; Wang et al., 2015; Zelina et al., 2014).”
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“…literature, our results support a model in which the loss of regulatory element activity in the motor cortex influences axon guidance properties of long-range projection neurons, which allow more robust connectivity between the cortex and the brainstem of vocal learning mammals ( 4 , 85 , 87 ).”
ResultSchizophrenia and Human Self-Domestication: An Evolutionary Linguistics Approach
Benítez‐Burraco, A., Pietro, L. D., Barba, M., & Lattanzi, W. (2017) · Brain Behavior and Evolution · doi:10.1159/000468506 · Cited by 37 · see citing works
“, 2014], and it is involved in the neural establishment of vocal learning abilities [Wang et al., 2015].”
BackgroundHerold, C., Paulitschek, C., Palomero‐Gallagher, N., Güntürkün, O., & Zilles, K. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24344 · Cited by 35 · see citing works
“However, it could be also possible that in vocal learning birds the arcopallium is located more medial in the forebrain and somewhat rotated medially compared to other avian species (Wang et al., 2015).”
BackgroundThe constitutive differential transcriptome of a brain circuit for vocal learning
Lovell, P. V., Huizinga, N. A., Friedrich, S. R., Wirthlin, M. E., & Mello, C. V. (2018) · BMC Genomics · doi:10.1186/s12864-018-4578-0 · Cited by 29 · see citing works
“This notion has been previously suggested as helping to establish the specificity of the RA-to-nXIIts projection [64], a connection critical for learned vocalizations, but it would require the preand post-synaptic localizations of SLITs and ROBOs, respectively.”
Boerma, T., ter Haar, S. M., Ganga, R., Wijnen, F. N. K., Blom, E., & Wierenga, C. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105398 · Cited by 29 · see citing works
“Variation in FOXP2 target genes or in binding partners of FOXP2 has been linked to language problems (Bates et al., 2011; den Hoed et al., 2021; Wang et al., 2015; Whitehouse et al., 2011).”
An oscillopathic approach to developmental dyslexia: From genes to speech processing
Jiménez-Bravo, M., Aguiar, V. M., & Benítez‐Burraco, A. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.03.048 · Cited by 28 · see citing works
Molecular specializations of deep cortical layer analogs in songbirds
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Narrowing the Genetic Causes of Language Dysfunction in the 1q21.1 Microduplication Syndrome
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“Interestingly, ROBO1 regulates interaural interaction in auditory pathways (71), and was co-opted for vocalization in songbirds as a component of the motor song output nucleus (72).”
BackgroundBirdsong as a window into language origins and evolutionary neuroscience
Aamodt, C., Farias-Virgens, M., & White, S. A. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0060 · Cited by 20 · see citing works
“The role of SLIT-ROBO signalling in vocal learning has been well characterized by Jarvis and co-workers [104].”
BackgroundEstrogen and sex-dependent loss of the vocal learning system in female zebra finches
Choe, H. N., Tewari, J., Zhu, K. W., Davenport, M. H., Matsunami, H., & Jarvis, E. D. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104911 · Cited by 20 · see citing works
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Emergence of sex-specific transcriptomes in a sexually dimorphic brain nucleus
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Pérez, C., Sawmiller, D. R., & Tan, J. (2016) · Neural Development · doi:10.1186/s13064-016-0066-x · Cited by 19 · see citing works
“In addition, a role for Slit/Robo malfunctioning in autism, dyslexia and other speech disorders is supported by a recent study showing that vocal learning birds (songbird, parrot and hummingbird) make a relatively rare connection between vocal learning circuits of the forebrain and brainstem vocal motor neurons, not s…”
BackgroundLei, H., Yan, Z., Sun, X., Zhang, Y., Wang, J., Ma, C., Xu, Q., Wang, R., Jarvis, E. D., & Sun, Z. (2017) · Brain and Language · doi:10.1016/j.bandl.2017.06.007 · Cited by 18 · see citing works
“The differential expression of ROBO1 and SLIT1 is developmentally regulated in the song learning production brain region in juvenile zebra finches, a songbird, during its critical period for song learning (Wang, 2011; Wang et al., 2015).”
BackgroundInfluentialSelf-citationSchuppe, E. R., Cantin, L. J., Chakraborty, M., Biegler, M. T., Jarvis, E. R., Chen, C.-C., Hara, E., Bertelsen, M., Witt, C. C., Jarvis, E., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001751 · Cited by 12 · see citing works
Avian models for brain mechanisms underlying altered social behavior in autism
Csillag, A., Ádám, Á., & Zachár, G. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.1032046 · Cited by 17 · see citing works
SRGAP2 and the gradual evolution of the modern human language faculty
Martins, P. T., Marí, M., & Boeckx, C. A. (2018) · Journal of Language Evolution · doi:10.1093/jole/lzx020 · Cited by 16 · see citing works
Convergent gene expression highlights shared vocal motor microcircuitry in songbirds and humansPreprint
Gedman, G. L., Biegler, M. T., Haase, B., Wirthlin, M. E., Fedrigo, O. D., Pfenning, A. R., & Jarvis, E. D. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.01.498177 · Cited by 15 · see citing works
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Buisan, R., Moriano, J., Andirkó, A., & Boeckx, C. A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.824740 · Cited by 14 · see citing works
Specificity in sociogenomics: Identifying causal relationships between genes and behavior
Ortiz, J. R., & Tollkühn, J. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104882 · Cited by 13 · see citing works
The pale spear‐nosed bat: A neuromolecular and transgenic model for vocal learning
Vernes, S. C., Devanna, P., Hörpel, S. G., van Tussenbroek, I. A., Firzlaff, U., Peter Hagoort, A., Hiller, M., Hoeksema, N., Hughes, G. M., Lavrichenko, K., et al. (2022) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14884 · Cited by 13 · see citing works
Korlach, J., Gedman, G. L., Kingan, S., Chin, C., Howard, J., Cantin, L. J., & Jarvis, E. (2017) · bioRxiv · doi:10.1101/103911 · Cited by 16 · see citing works
“Recently, SLIT1 was shown to have convergent specialized down-regulated expression compared to the surrounding brain region in the RA song nucleus of all independently evolved vocal learning bird lineages and in the analogous human LMC (Pfenning et al. 2014; Wang et al. 2014) (Suppl.”
BackgroundBrain activity underlying American crow processing of encounters with dead conspecifics
Swift, K. N., Marzluff, J. M., Templeton, C. N., Shimizu, T., & Cross, D. J. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112546 · Cited by 10 · see citing works
Cell type specializations of the vocal-motor cortex in songbirds
Nevue, A. A., Zemel, B. M., Friedrich, S. R., von Gersdorff, H., & Mello, C. V. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113344 · Cited by 9 · see citing works
“99 Instead, our data suggest that SLIT-ROBO mechanisms are more likely involved in establishing local inhibitory networks in RA.”
Failure to attune to language predicts autism in high risk infants
Denisova, K. (2019) · Brain and Language · doi:10.1016/j.bandl.2019.04.002 · Cited by 9 · see citing works
Animal models of developmental dyslexia: Where we are and what we are missing
Lampis, V., Ventura, R., Segni, M. D., Marino, C., D'Amato, F. R., & Mascheretti, S. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.022 · Cited by 9 · see citing works
FOXP2 and language alterations in psychiatric pathology
Castro-Martínez, X. H., Moltó, M. D., Morales-Marín, M. E., Flóres-Lázaro, J. C., González-Fernández, J., Gutiérrez-Nájera, N., Alvarez-Amado, D. E., & Sánchez, J. H. N. (2019) · Salud Mental · doi:10.17711/sm.0185-3325.2019.039 · Cited by 8 · see citing works
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Does a Vertebrate Morphotype of Pallial Subdivisions Really Exist?
Yamamoto, K., Estienne, P., & Bloch, S. (2024) · Brain Behavior and Evolution · doi:10.1159/000537746 · Cited by 7 · see citing works
“This has often been compared to the projections from the motor cortex to the nucleus ambiguus that control larynx muscles in mammalian vocal learners [47].”
Approaching motor and language deficits in autism from below: a biolinguistic perspective
Benítez‐Burraco, A., & Boeckx, C. A. (2015) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2015.00025 · Cited by 7 · see citing works
“As noted by Wang et al. (2015) this may be due to the involvement of the ROBO proteins and their ligand SLITs, which play a central role in the organization of the specialized forebrain circuits that control vocal learning, specifically, the forebrain part that connects to brainstem vocal motor…”
BackgroundDynamic transcriptome landscape in the song nucleus HVC between juvenile and adult zebra finches
Shi, Z., Zhang, Z., Schaffer, L., Huang, Z., Fu, L., Head, S. R., Gaasterland, T., Wang, X., & Li, X.-C. (2020) · Advanced Genetics · doi:10.1002/ggn2.10035 · Cited by 5 · see citing works
“expressed in HVC and to be developmentally regulated in RA, the downstream nucleus to which HVC connects.(25,46) Other members of the axon guidance term enriched in 45 d HVC include genes coding”
BackgroundThe role of sex chromosomes and sex hormones in vocal learning systems.
Choe, H., & Jarvis, E. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.104978 · Cited by 6 · see citing works
Animal models of developmental dyslexia
Galaburda, A. M. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.981801 · Cited by 6 · see citing works
“, 2020) and vocal learning in animals (Wang et al., 2015); the gene has been associated with increased interneuron migration into the cerebral cortex, as well as altered inter and intrahemispheric connectivity (Andrews et al.”
BackgroundSchizophrenia and human self-domestication: an evolutionary linguistics approachPreprint
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Are feralization and domestication truly mirror processes?
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News Feature: Singing in the brain
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The genomics of the domestication syndrome in a songbird model species
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“…nuclei RA and HVC and in the brainstem motor nucleus nXIIts is suggested to facilitate the targeting of ROBO-expressing terminals and guide the development of neuronal projections from HVC to RA, as well as direct projections from RA to nXIIts, a connection critical for learned vocalizations 33 .”
Avian vocal learning and the evolution of language-relevant communication
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A genetic window to auditory-verbal problems in bipolar disorder
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The Evolution of Language and Speech
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Domain-general perspectives on the neurocognitive specialization of language
Castillo, G. (2017) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
Are feralization and domestication truly mirror processes?Preprint
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The trade-off between vocal learning and dexterity: a balancing actPreprint
Martins, P. T., & Boeckx, C. A. (2023) · doi:10.32942/x2f88f
Enhancing cortico-motoneuronal projections for vocalization in micePreprint
Boyd, J. L., Kuper, L. C., Waidmann, E. N., Yang, V. H. Y., & Jarvis, E. D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.14.618267
- Authors
- Wang, R., Chen, C., Hara, E., Rivas, M. V., Roulhac, P. L., Howard, J. T., Chakraborty, M., Audet, J., & Jarvis, E. D.
- Affiliations
- Howard Hughes Medical Institute (US)
- McGill University (CA)
- Corresponding author
- Jarvis, Erich D.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2014-12-30
- Volume
- 523
- Issue
- 6
- Pages
- 892-906
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- PMC
- PMC4329046
- OpenAlex
- W1552398907
- Cited by
- 74
- References
- 51
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 4 · 2023: 3 · 2022: 9 · 2021: 7 · 2020: 10 · 2019: 8 · 2018: 6 · 2017: 11 · 2016: 6 · 2015: 7 · 2014: 1
- FWCI
- 7.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Journal of Comparative Neurology (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
- Funders
- NIH Office of the Director (DP1 OD000448)
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- vocal learning, axon guidance, convergent evolution, songbirds, parrots, hummingbirds, Slit1, ROBO1, vocal plasticity, autism spectrum disorder, dyslexia, speech sound disorders, gene expression regulation
- MeSH terms
- Roundabout Proteins, Age Factors, Animals, Axons, Birds, Brain, Female, Gene Expression Regulation, Glycoproteins, Learning, Male, Mice, Inbred C57BL, Nerve Tissue Proteins, Neurons, Receptors, Immunologic, RNA, Messenger, Vocalization, Animal, Mice
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