Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques
Open accessAbstract
Over the course of ontogenesis, the human brain and human cognitive abilities develop in parallel, resulting in a phenotype strikingly distinct from that of other primates. Here, we used microarrays and RNA-sequencing to examine human-specific gene expression changes taking place during postnatal brain development in the prefrontal cortex and cerebellum of humans, chimpanzees, and rhesus macaques. We show that the most prominent human-specific expression change affects genes associated with synaptic functions and represents an extreme shift in the timing of synaptic development in the prefrontal cortex, but not the cerebellum. Consequently, peak expression of synaptic genes in the prefrontal cortex is shifted from <1 yr in chimpanzees and macaques to 5 yr in humans. This result was supported by protein expression profiles of synaptic density markers and by direct observation of synaptic density by electron microscopy. Mechanistically, the human-specific change in timing of synaptic development involves the MEF2A-mediated activity-dependent regulatory pathway. Evolutionarily, this change may have taken place after the split of the human and the Neanderthal lineages.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Comparison with the chimpanzee also indicates human neoteny, although less pronounced.
“comparison with the chimpanzee also indicates human neoteny, although less pronounced”
From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Liu et al., 2012
The paper’s Discussion reports delayed prefrontal cortical synaptic development in humans relative to chimpanzees, supporting the comparison as evidence of human neoteny. It does not establish that the delay relative to chimpanzees is less pronounced than the delay relative to macaques; it describes synaptic-gene expression in both comparison species as peaking shortly after birth. No page number is available in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredChanges to regulatory regions may have had important functional consequences for the emergence of the human cognitive phenotype.
“suggesting that changes to regulatory regions may have had important functional consequences for the emergence of the human cognitive phenotype.”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Liu et al., 2012
There are significant differences between humans and chimpanzees in the cortical expression of glutamate receptor genes.
“Despite this high structural conservation, there are significant differences between humans and chimpanzees in the cortical expression of glutamate receptor genes (Liu et al., 2012;Muntané et al., 2015), suggesting that changes to regulatory regions may have had important functional consequences for the emergence of the human cognitive phenotype.”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Liu et al., 2012
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
KEGG for linking genomes to life and the environment
Kanehisa, M. I., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S., Tokimatsu, T., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm882 · Cited by 6,828 · see citing works
A draft sequence of the Neandertal genome
Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U., Kircher, M., Patterson, N., Li, H., Zhai, W., Fritz, M. H.-Y., et al. (2010) · Science · doi:10.1126/science.1188021 · Cited by 4,318 · see citing works
Self-citation(1977) · Cited by 4,052 · see citing works
Malenka, R. C., & Bear, M. F. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.012 · Cited by 3,968 · see citing works
Origins of Human Communication
Tomasello, M. (2008) · The MIT Press eBooks · doi:10.7551/mitpress/7551.001.0001 · Cited by 3,205 · see citing works
King, M.-C., & Wilson, A. C. (1975) · Science · doi:10.1126/science.1090005 · Cited by 2,815 · see citing works
Origins of human communication
(2009) · Choice Reviews Online · doi:10.5860/choice.46-3671 · Cited by 2,235 · see citing works
Long-Term Potentiation and Memory
Lynch, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00014.2003 · Cited by 2,001 · see citing works
Genetic history of an archaic hominin group from Denisova Cave in Siberia
Reich, D., Green, R. E., Kircher, M., Krause, J., Patterson, N., Durand, E. Y., Viola, B., Briggs, A. W., Stenzel, U., Johnson, P. L. F., et al. (2010) · Nature · doi:10.1038/nature09710 · Cited by 1,991 · see citing works
Self-citationA molecular timescale for vertebrate evolution
Kumar, S., & Hedges, S. B. (1998) · Nature · doi:10.1038/31927 · Cited by 1,936 · see citing works
Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways
Hardingham, G. E., Fukunaga, Y., & Bading, H. (2002) · Nature Neuroscience · doi:10.1038/nn835 · Cited by 1,686 · see citing works
Grandmothering, menopause, and the evolution of human life histories
Hawkes, K., O’Connell, J. F., Jones, N. G. B., Alvarez, H., & Charnov, E. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.1336 · Cited by 1,343 · see citing works
Whole-Genome Patterns of Common DNA Variation in Three Human Populations
Hinds, D., Stuve, L., Nilsen, G. B., Halperin, E., Eskin, E., Ballinger, D., Frazer, K., & Cox, D. (2005) · Science · doi:10.1126/science.1105436 · Cited by 1,245 · see citing works
Linked Regularities in the Development and Evolution of Mammalian Brains
Finlay, B. L., & Darlington, R. B. (1995) · Science · doi:10.1126/science.7777856 · Cited by 1,217 · see citing works
Plasticity in the human central nervous system
Cooke, S. F. (2006) · Brain · doi:10.1093/brain/awl082 · Cited by 1,195 · see citing works
Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex
Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986) · Science · doi:10.1126/science.3952506 · Cited by 1,133 · cited 10× · see citing works
“This finding might be linked to earlier observations from stereological studies showing that synaptic density in the PFC peaks around 4–5 yr of age in humans but within the first months in macaques (Rakic et al. 1986; Huttenlocher and Dabholkar 1997).”
BackgroundMethodResultInfluentialThe primate cortico-cerebellar system: anatomy and function
Ramnani, N. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1953 · Cited by 1,011 · see citing works
Functional brain development in humans
Johnson, M. H. (2001) · Nature Reviews Neuroscience · doi:10.1038/35081509 · Cited by 980 · see citing works
Human prefrontal cortex: processing and representational perspectives
Wood, J. N., & Grafman, J. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1033 · Cited by 721 · see citing works
Chen, F.-C., & Li, W. (2001) · The American Journal of Human Genetics · doi:10.1086/318206 · Cited by 720 · see citing works
MEF2: a calcium-dependent regulator of cell division, differentiation and death
McKinsey, T. A., Zhang, C. L., & Olson, E. N. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(01)02031-x · Cited by 691 · see citing works
A database of vertebrate longevity records and their relation to other life‐history traits
de Magalhães, J. P., & Costa, J. S. (2009) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2009.01783.x · Cited by 577 · see citing works
Activity-Dependent Regulation of MEF2 Transcription Factors Suppresses Excitatory Synapse Number
Flavell, S. W., Cowan, C. W., Kim, T.-K., Greer, P. L., Lin, Y., Paradis, S., Griffith, E. C., Hu, L. S., Chen, C., & Greenberg, M. E. (2006) · Science · doi:10.1126/science.1122511 · Cited by 573 · see citing works
Neuronal Activity-Dependent Cell Survival Mediated by Transcription Factor MEF2
Mao, Z., Bonni, A., Xia, F., Nadal-Vicens, M. F., & Greenberg, M. E. (1999) · Science · doi:10.1126/science.286.5440.785 · Cited by 505 · see citing works
Elevated gene expression levels distinguish human from non-human primate brains
Cáceres, M., Lachuer, J., Zapala, M. A., Redmond, J. C., Kudo, L., Geschwind, D. H., Lockhart, D. J., Preuss, T. M., & Barlow, C. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2135499100 · Cited by 491 · see citing works
A Calcium-Regulated MEF2 Sumoylation Switch Controls Postsynaptic Differentiation
Shalizi, A., Gaudilliere, B. L., Yuan, Z., Stegmüller, J., Shirogane, T., Ge, Q., Tan, Y. L., Schulman, B. A., Harper, J. W., & Bonni, A. (2006) · Science · doi:10.1126/science.1122513 · Cited by 456 · see citing works
Flavell, S. W., Kim, T.-K., Gray, J. M., Harmin, D. A., Hemberg, M., Hong, E. J., Markenscoff-Papadimitriou, E., Bear, D. M., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.11.029 · Cited by 440 · see citing works
Transcriptional neoteny in the human brain
Somel, M., Franz, H., Zheng, Y., Lorenc, A., Guo, S., Giger, T., Kelso, J. F., Nickel, B., Dannemann, M., Bahn, S., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900544106 · Cited by 409 · see citing works
Self-citationBrain growth, life history, and cognition in primate and human evolution
LEIGH, S. R. (2004) · American Journal of Primatology · doi:10.1002/ajp.20012 · Cited by 374 · cited 3× · see citing works
“Humans are born in an altricial state and undergo both rapid and extended brain growth compared with that of macaques and chimpanzees (Leigh 2004).”
BackgroundInfluentialAges of eruption of primate teeth: A compendium for aging individuals and comparing life histories
Smith, B. H., Crummett, T. L., & Brandt, K. L. (1994) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330370608 · Cited by 364 · see citing works
Genomewide Comparison of DNA Sequences between Humans and Chimpanzees
Ebersberger, I., Metzler, D., Schwarz, C., & Pääbo, S. (2002) · The American Journal of Human Genetics · doi:10.1086/340787 · Cited by 343 · see citing works
Self-citationEvolution of primate gene expression
Khaitovich, P., Enard, W., Lachmann, M., & Pääbo, S. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1940 · Cited by 341 · see citing works
Self-citationGenetics and the making of Homo sapiens
Carroll, S. B. (2003) · Nature · doi:10.1038/nature01495 · Cited by 340 · see citing works
Dental evidence for ontogenetic differences between modern humans and Neanderthals
Smith, T. M., Tafforeau, P., Reid, D. J., Pouech, J., Lazzari, V., Zermeno, J. P., Guatelli-Steinberg, D., Olejniczak, A. J., Hoffman, A., Radovčić, J., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010906107 · Cited by 331 · see citing works
Practical Regression and Anova using R
Faraway, J. J. (2002) · Cited by 331 · see citing works
Hunt, C., Schenker, L. J., & Kennedy, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-04-01380.1996 · Cited by 313 · see citing works
Barbosa, A. C., Kim, M.-S., Ertunc, M., Adachi, M., Nelson, E. D., McAnally, J., Richardson, J. A., Kavalali, E. T., Monteggia, L. M., Bassel-Duby, R., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802679105 · Cited by 303 · see citing works
Theory of mind: evolutionary history of a cognitive specialization
Povinelli, D. J., & Preuss, T. M. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93939-u · Cited by 294 · see citing works
Cocaine Regulates MEF2 to Control Synaptic and Behavioral Plasticity
Pulipparacharuvil, S., Renthal, W., Hale, C. F., Taniguchi, M., Xiao, G., Kumar, A., Russo, S. J., Sikder, D., Dewey, C. M., Davis, M. M., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.020 · Cited by 281 · see citing works
Davis, S., Bozon, B., & Laroche, S. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00421-7 · Cited by 281 · see citing works
Scalable architecture in mammalian brains
Clark, D. A., Mitra, P. P., & Wang, S. S.-H. (2001) · Nature · doi:10.1038/35075564 · Cited by 276 · see citing works
Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation
Lyons, G., Micales, B. K., Schwarz, J. J., Martin, J., & Olson, E. N. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05727.1995 · Cited by 271 · see citing works
Glantz, L. A., Gilmore, J. H., Hamer, R. M., Lieberman, J. A., & Jarskog, L. F. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.06.036 · Cited by 270 · see citing works
Masliah, E., Terry, R. D., Alford, M. F., & DeTeresa, R. M. (1990) · Journal of Histochemistry & Cytochemistry · doi:10.1177/38.6.2110586 · Cited by 267 · see citing works
Molecular genetics of human microcephaly
Mochida, G. H., & Walsh, C. A. (2001) · Current Opinion in Neurology · doi:10.1097/00019052-200104000-00003 · Cited by 239 · see citing works
MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates
Somel, M., Liu, X., Tang, L., Yan, Z., Hu, H., Guo, S., Jiang, X., Zhang, X., Xu, G., Xie, G., et al. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001214 · Cited by 232 · see citing works
Self-citationNatural selection on gene expression
Gilad, Y., Oshlack, A., & Rifkin, S. A. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.06.002 · Cited by 218 · see citing works
Human and nonhuman primate brains: Are they allometrically scaled versions of the same design?
Rilling, J. K. (2006) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.20095 · Cited by 214 · see citing works
Spatial Organization of Neurons in the Frontal Pole Sets Humans Apart from Great Apes
Semendeferi, K., Teffer, K., Buxhoeveden, D. P., Park, M. S., Bludau, S., Amunts, K., Travis, K., & Buckwalter, J. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq191 · Cited by 210 · see citing works
Liu, L., Cavanaugh, J. E., Wang, Y., Sakagami, H., Mao, Z., & Xia, Z. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1332804100 · Cited by 161 · see citing works
In Search of the Neanderthals: Solving the Puzzle of Human Origins
Stringer, C. B., & Gamble, C. (1993) · ePrints Soton (University of Southampton) · Cited by 128 · see citing works
Egr3, a synaptic activity regulated transcription factor that is essential for learning and memory
Li, L., Yun, S. H., Keblesh, J., Trommer, B. L., Xiong, H., Radulovic, J., & Tourtellotte, W. G. (2007) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2007.02.004 · Cited by 124 · cited 2× · see citing works
“potentiation (Davis et al. 2003; Flavell et al. 2006; Shalizi et al. 2006; Li et al. 2007), raising the possibility that module 1 genes have roles in synaptic development and neuronal functions.”
BackgroundPenin, X., Berge, C., & Baylac, M. (2002) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10044 · Cited by 124 · see citing works
A handbook of living primates: morphology, ecology and behaviour of nonhuman primates
Napier, J. R., & Napier, P. H. (1967) · Medical Entomology and Zoology · Cited by 116 · see citing works
Bogin, B. A. (2009) · American Journal of Human Biology · doi:10.1002/ajhb.20895 · Cited by 115 · see citing works
Increased Cortical Expression of Two Synaptogenic Thrombospondins in Human Brain Evolution
Cáceres, M., Suwyn, C. R., Maddox, M., Thomas, J. W., & Preuss, T. M. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl140 · Cited by 114 · see citing works
Rapid metabolic evolution in human prefrontal cortex
Fu, X., Giavalisco, P., Liu, X., Catchpole, G., Fu, N., Ning, Z., Guo, S., Zheng, Y., Somel, M., Pääbo, S., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019164108 · Cited by 99 · see citing works
Self-citationShalizi, A., Lehtinen, M. K., Gaudilliere, B. L., Donovan, N., Han, J., Konishi, Y., & Bonni, A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-19-07326.2003 · Cited by 97 · see citing works
An evolutionarily adaptive neural architecture for social reasoning
Barbey, A. K., Krüeger, F., & Grafman, J. H. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.09.001 · Cited by 61 · see citing works
Didier, M., Roux, P., Piechaczyk, M., Verrier, B., Bockaert, J., & Pin, J. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90790-8 · Cited by 59 · see citing works
Reichert, H. (2008) · Biology Letters · doi:10.1098/rsbl.2008.0337 · Cited by 56 · see citing works
The Heterochronic Evolution of Primate Cognitive Development
Langer, J. (2006) · Biological Theory · doi:10.1162/biot.2006.1.1.41 · Cited by 33 · see citing works
Yuan, Y., Chen, Y. P., Ni, S., Xu, A. G., Tang, L., Vingron, M., Somel, M., & Khaitovich, P. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-347 · Cited by 33 · see citing works
Self-citationPääbo, S. (1999) · Trends in Cell Biology · doi:10.1016/s0962-8924(99)01688-8 · Cited by 18 · see citing works
Self-citationPääbo, S. (1999) · PubMed · Cited by 8 · see citing works
Self-citationGavan, J. A. (1969) · American Anthropologist · doi:10.1525/aa.1969.71.2.02a00550 · Cited by 2 · see citing works
Evolutionary hypotheses for human childhood
Bogin, B. (1997) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(1997)25+
Kaplan (2000) · doi:10.1002/1520-6505(2000)9:4
Huttenlocher (1997) · doi:10.1002/(sici)1096-9861(19971020)387:2
Flagged first, then by citations
Research works printed but not linked: 1
- McNamara KJ. 1997. Shapes of time. Johns Hopkins University Press, Baltimore.
Cited by
Sorted by citations
Evolution of the Human Nervous System Function, Structure, and Development
Sousa, A. M. M., Meyer, K. A., Santpere, G., Gulden, F. O., & Sestan, N. (2017) · Cell · doi:10.1016/j.cell.2017.06.036 · Cited by 517 · see citing works
Araki, Y., Zeng, M., Zhang, M., & Huganir, R. L. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.023 · Cited by 271 · see citing works
A Quantitative Framework to Evaluate Modeling of Cortical Development by Neural Stem Cells
Stein, J. L., de la Torre-Ubieta, L., Tian, Y., Parikshak, N. N., Hernández, I. A., Marchetto, M. C., Baker, D. K., Lu, D., Hinman, C. R., Lowe, J. K., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.035 · Cited by 201 · see citing works
Widespread splicing changes in human brain development and aging
Mazin, P., Xiong, J., Liu, X., Yan, Z., Zhang, X., Li, M., He, L., Somel, M., Yuan, Y., Phoebe Chen, Y., et al. (2013) · Molecular Systems Biology · doi:10.1038/msb.2012.67 · Cited by 216 · see citing works
Self-citationLinaro, D., Vermaercke, B., Iwata, R., Ramaswamy, A., Davis, B. A., Boubakar, L., Libé-Philippot, B., Bilheu, A., Bruyne, L. D., Gall, D., et al. (2019) · doi:10.1101/626218 · Cited by 210 · see citing works
“, Zhang, B., Arckens, L., and Chino, Y.M. (2010). Receptive-field properties of V1 and V2 neurons in mice and macaque monkeys.”
BackgroundInfluentialBrain Plasticity and Human Evolution
Sherwood, C. C., & Gómez-Robles, A. (2017) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-102215-100009 · Cited by 170 · see citing works
Developmental mechanisms underlying the evolution of human cortical circuits
Vanderhaeghen, P., & Polleux, F. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00675-z · Cited by 173 · see citing works
Evolution of genetic and genomic features unique to the human lineage
O'Bleness, M., Searles, V. B., Varki, A., Gagneux, P., & Sikela, J. M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3336 · Cited by 168 · see citing works
Bianchi, S., Stimpson, C. D., Duka, T., Larsen, M. D., Janssen, W. G. M., Collins, Z., Bauernfeind, A. L., Schapiro, S. J., Baze, W. B., McArthur, M. J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301224110 · Cited by 136 · see citing works
Species-specific maturation profiles of human, chimpanzee and bonobo neural cells
Marchetto, M. C., Hrvoj-Mihic, B., Kerman, B. E., Yu, D. X., Vadodaria, K. C., Linker, S. B., Narvaiza, I., Santos, R., Denli, A. M., Mendes, A. P., et al. (2019) · eLife · doi:10.7554/elife.37527 · Cited by 132 · see citing works
A catalog of single nucleotide changes distinguishing modern humans from archaic hominins
Kuhlwilm, M., & Boeckx, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-44877-x · Cited by 108 · see citing works
Disruption of an Evolutionarily Novel Synaptic Expression Pattern in Autism
Liu, X., Han, D., Somel, M., Jiang, X., Hu, H., Guijarro, P., Zhang, N., Mitchell, A., Halene, T., Ely, J. J., et al. (2016) · PLOS Biology · doi:10.1371/journal.pbio.1002558 · Cited by 87 · see citing works
Self-citationA cross-species proteomic map reveals neoteny of human synapse development
Wang, L., Pang, K., Zhou, L., Cebrián-Silla, A., González-Granero, S., Wang, S., Bi, Q., White, M. L., Ho, B., Li, J., et al. (2023) · Nature · doi:10.1038/s41586-023-06542-2 · Cited by 82 · see citing works
Human neuronal maturation comes of age: cellular mechanisms and species differences
Wallace, J. L., & Pollen, A. A. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00760-3 · Cited by 82 · see citing works
A cross-species proteomic map reveals neoteny of human synapse development
Wang, L., Pang, K., Zhou, L., Cebrián-Silla, A., González-Granero, S., Wang, S., Bi, Q., White, M. L., Ho, B., Li, J., et al. (2022) · doi:10.1101/2022.10.24.513541 · Cited by 82 · see citing works
Cellular and Molecular Mechanisms Linking Human Cortical Development and Evolution
Libé-Philippot, B., & Vanderhaeghen, P. (2021) · Annual Review of Genetics · doi:10.1146/annurev-genet-071719-020705 · Cited by 78 · see citing works
Pruunsild, P., Bengtson, C. P., & Bading, H. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.018 · Cited by 78 · see citing works
Xiao, X., Moreno-Moral, A., Rotival, M., Bottolo, L., & Petretto, E. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004006 · Cited by 63 · see citing works
Climbing Brain Levels of Organisation from Genes to Consciousness
Changeux, J.-P. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.01.004 · Cited by 61 · see citing works
Glutamate receptors in domestication and modern human evolution
O’Rourke, T., & Boeckx, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.004 · Cited by 50 · see citing works
From Human Pluripotent Stem Cells to Cortical Circuits
Astick, M., & Vanderhaeghen, P. (2018) · Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2018.02.011 · Cited by 34 · see citing works
Isochronic development of cortical synapses in primates and mice
Wildenberg, G., Li, H., Sampathkumar, V., Sorokina, A., & Kasthuri, N. (2023) · Nature Communications · doi:10.1038/s41467-023-43088-3 · Cited by 31 · see citing works
Hrvoj-Mihic, B., Hanson, K. L., Lew, C. H., Stefanacci, L., Jacobs, B., Bellugi, U., & Semendeferi, K. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00419 · Cited by 21 · see citing works
- Authors
- Liu, X., Somel, M., Tang, L., Yan, Z., Jiang, X., Guo, S., Yuan, Y., He, L., Oleksiak, A., Zhang, Y., Li, N., Hu, Y., Chen, W., Qiu, Z., Pääbo, S., & Khaitovich, P.
- Affiliations
- Chinese Academy of Sciences (CN)
- La Trobe University (AU)
- Max Delbrück Center (DE)
- Max Planck Institute for Evolutionary Anthropology (DE)
- ORCID
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2012-02-02
- Volume
- 22
- Issue
- 4
- Pages
- 611-622
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC3317144
- OpenAlex
- W2105507567
- Cited by
- 251
- References
- 71
- Citations by year
- 2026: 14 · 2025: 10 · 2024: 12 · 2023: 23 · 2022: 9 · 2021: 14 · 2020: 32 · 2019: 19 · 2018: 15 · 2017: 19 · 2016: 22 · 2015: 18 · 2014: 18 · 2013: 20 · 2012: 6
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome Research (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- OpenMETU (Middle East Technical University) (submittedVersion, cc-by-nc-nd)
- HighWire Press Open Archive (submittedVersion)
- Funders
- European Molecular Biology Organization
- National Natural Science Foundation of China
- Chinese Academy of Sciences (KSCX2-YW-R)
- Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences
- Ministry of Science and Technology of the People's Republic of China (2011CBA00400)
- Universität Zürich
- Directorate for Biological Sciences
- National Key Research and Development Program of China (2011CBA00400)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- human brain evolution, synaptic development, prefrontal cortex, cerebellum, chimpanzees, rhesus monkeys, synaptic genes, synaptic density, MEF2A, activity-dependent regulation, postnatal brain development
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Animals, Cerebellum, Child, Child, Preschool, Pan troglodytes, Humans, Infant, Infant, Newborn, Macaca mulatta, Middle Aged, Neuromuscular Junction, Species Specificity, Synapses, Prefrontal Cortex, Sequence Analysis, RNA, Gene Expression Regulation, Developmental, Evolution, Molecular, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Young Adult
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
