A human-specific modifier of cortical connectivity and circuit function
Open accessPublished version of a preprint
Abstract
The cognitive abilities that characterize humans are thought to emerge from unique features of the cortical circuit architecture of the human brain, which include increased cortico-cortical connectivity. However, the evolutionary origin of these changes in connectivity and how they affected cortical circuit function and behaviour are currently unknown. The human-specific gene duplication SRGAP2C emerged in the ancestral genome of the Homo lineage before the major phase of increase in brain size 1,2. SRGAP2C expression in mice increases the density of excitatory and inhibitory synapses received by layer 2/3 pyramidal neurons (PNs)3-5. Here we show that the increased number of excitatory synapses received by layer 2/3 PNs induced by SRGAP2C expression originates from a specific increase in local and long-range cortico-cortical connections. Mice humanized for SRGAP2C expression in all cortical PNs displayed a shift in the fraction of layer 2/3 PNs activated by sensory stimulation and an enhanced ability to learn a cortex-dependent sensory-discrimination task. Computational modelling revealed that the increased layer 4 to layer 2/3 connectivity induced by SRGAP2C expression explains some of the key changes in sensory coding properties. These results suggest that the emergence of SRGAP2C at the birth of the Homo lineage contributed to the evolution of specific structural and functional features of cortical circuits in the human cortex.
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SRGAP2B/C downregulation had no detectable impact on cortical neuron integration and fate determination.
“These data indicate that SRGAP2B/C downregulation had no detectable impact on cortical neuron integration and fate determination, in line with the data obtained in mouse CPNs following downregulation of SRGAP2 or overexpression of SRGAP2C.24,31”
From Synaptic neoteny of human cortical neurons requires species-specific balancing of SRGAP2-SYNGAP1 cross-inhibition (2024) · cites this paper as [31]
The ‘Increased connectivity in SRGAP2C mice’ section reports that cortical depth did not differ between genotypes, which supports a limited point about the positioning of mouse cortical pyramidal neurons. It does not report a test of neuronal fate determination or establish that cortical neuron integration was unaffected; instead, it reports increased synaptic inputs with SRGAP2C expression. (LLM, conf=0.76)
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- Authors
- Schmidt, E. R. E., Zhao, H. T., Park, J. M., Dipoppa, M., Monsalve-Mercado, M. M., Dahan, J. B., Rodgers, C. C., Lejeune, A., Hillman, E. M. C., Miller, K. D., Bruno, R. M., & Polleux, F.
- Affiliations
- Medical University of South Carolina (US)
- Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
- Corresponding author
- Polleux, Franck
- ORCID
- Venue
- Nature
- Published
- 2021-10-27
- Volume
- 599
- Issue
- 7886
- Pages
- 640-644
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC9161439
- OpenAlex
- W3210775554
- Cited by
- 82
- References
- 76
- Citations by year
- 2026: 7 · 2025: 14 · 2024: 22 · 2023: 21 · 2022: 13 · 2021: 3 · 2020: 2
- FWCI
- 8.33
- Type
- journal article
- Language
- en
- Update notices
- correction (2022-01-06)
- Open access
- green
- doi.org
- Licence
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Lirias (submittedVersion)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (825.14.017)
- National Institutes of Health (1uf1ns108213-01)
- National Institute on Aging (F99AG073558)
- National Institute of Mental Health (RF1MH114276)
- National Institute of General Medical Sciences (R01GM114276)
- National Institute of Neurological Disorders and Stroke (F32NS096819, UF1 NS108213, U19NS104649, R01NS067557, R01NS094659, U19NS107613, R01NS069679, R01NS063226, K99NS109323)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- gene duplication, human evolution, cortical connectivity, layer 2/3 pyramidal neurons, excitatory synapses, corticocortical connections, sensory coding, humanized mice, cognitive evolution
- MeSH terms
- Animals, Cerebral Cortex, Discrimination, Psychological, Female, Humans, Male, Mice, Transgenic, Neural Pathways, Organ Size, Synapses, Pyramidal Cells, Calcium Signaling, GTPase-Activating Proteins, Mice
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 ›
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