Modeling the evolution of cortico‐cerebellar systems in primates
Abstract
Although it is commonly accepted that brains work as functionally distributed systems in which interconnected structures work together in processing particular types of information, few studies have investigated the evolution of functionally specialized neural systems across many different lineages. MR‐related research has provided in‐depth information on connectivity patterns, but because of its focus on particular species, it has given only indicative clues about evolutionary patterns shaping brain organization across primates. Here, we combine depth with breadth of analysis by investigating patterns of covarying size evolution in substructures of the cortico‐cerebellar system across 19 anthropoid species spanning 35 million years of divergent evolution. Results demonstrate two distinct patterns of size covariation in substructures of the cortico‐cerebellar system, suggesting neural systems involving profuse cortico‐cerebellar connections are a major factor in explaining the evolution of anthropoid brain organization. We set out an evolutionary model of relative cortico‐cerebellar expansion and provide a detailed picture of its branch‐specific evolutionary history suggesting the ape radiation is the clade with the strongest and most consistent evolutionary history in relative (frontal) cortico‐cerebellar expansion.
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There is a striking correspondence between the patterns of correlated evolution among specific components of the cortico-cerebellar system and their anatomical connectivity, down to the level of individual nuclei.
“Second, there is a striking correspondence between the patterns of correlated evolution among specific components of the cortico-cerebellar system and their anatomical connectivity, down to the level of individual nuclei [62,67].”
From Embodied cognitive evolution and the cerebellum (2012) · cites this paper as [62]
Recent allometric analyses reveal that, although absolute and proportional frontal region size increased rapidly in hominins, this change was associated with size increase in other areas and whole brain size, rather than with specialization for enlarged frontal lobes specifically.
“Recent allometric analyses reveal that, although absolute and proportional frontal region size increased rapidly in hominins, this change was associated with size increase in other areas and whole brain size, rather than with specialization for enlarged frontal lobes specifically [57,61–63].”
From Embodied cognitive evolution and the cerebellum (2012) · cites this paper as [62]
The importance of the frontal lobes in cognitive evolution needs to be interpreted in terms of the areas with which they connect and with which they have co-evolved, including the cerebellum.
“This does not suggest that the frontal lobes were unimportant in cognitive evolution, just that their importance needs to be interpreted in terms of the areas with which they connect and with which they have co-evolved, including the cerebellum [61,62].”
From Embodied cognitive evolution and the cerebellum (2012) · cites this paper as [62]
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Self-citationJacobs, B., Johnson, N. L., Wahl, D., Schall, M., Maseko, B. C., Lewandowski, A. H., Raghanti, M. A., Wicinski, B. A., Butti, C., Hopkins, W. D., et al. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00024 · Cited by 52 · see citing works
Effects of cranial integration on hominid endocranial shape
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Diversity and evolution of cerebellar folding in mammals
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Variation in the strength of allometry drives rates of evolution in primate brain shape
Sansalone, G., Allen, K. L., Ledogar, J. A., Ledogar, S. H., Mitchell, D. R., Profico, A., Castiglione, S., Melchionna, M., Serio, C., Mondanaro, A., et al. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.0807 · Cited by 34 · see citing works
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Laterality and the evolution of the prefronto‐cerebellar system in anthropoids
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Shine, J. M., & Shine, R. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00090 · Cited by 27 · see citing works
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Sendhilnathan, N., Bostan, A. C., Strick, P. L., & Goldberg, M. E. (2024) · Nature Communications · doi:10.1038/s41467-024-46281-0 · Cited by 25 · see citing works
The coevolution of play and the cortico-cerebellar system in primates
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MacLeod, C. E. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00008-8 · Cited by 21 · see citing works
Magielse, N., Toro, R., Steigauf, V., Abbaspour, M., Eickhoff, S. B., Heuer, K., & Valk, S. L. (2023) · Communications Biology · doi:10.1038/s42003-023-05553-z · Cited by 18 · see citing works
Three brain collections for comparative neuroanatomy and neuroimaging
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Contextualising primate origins – an ecomorphological framework
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Self-citationThe Evolution of the Frontal Lobe in Humans
Parks, A. N., & Smaers, J. (2018) · Springer eBooks · doi:10.1007/978-4-431-56582-6_14 · Cited by 10 · see citing works
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Stacho, M., Häusler, A. N., Brandstetter, A., Iannilli, F., Mohlberg, H., Schiffer, C., Smaers, J. B., & Amunts, K. (2024) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2024.1331305 · Cited by 11 · see citing works
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Koziol, L. F., Barker, L. A., Joyce, A. W., & Hrin, S. (2014) · Applied Neuropsychology Child · doi:10.1080/21622965.2014.946804 · Cited by 9 · see citing works
Large-Scale Brain Systems and Subcortical Relationships: Practical Applications
Koziol, L. F., Barker, L. A., Hrin, S., & Joyce, A. W. (2014) · Applied Neuropsychology Child · doi:10.1080/21622965.2014.946809 · Cited by 8 · see citing works
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Dellatolas, G., & Câmara‐Costa, H. (2020) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64150-2.00023-x · Cited by 8 · see citing works
Gómez‐Robles, A., Reyes, L. D., & Sherwood, C. C. (2017) · Springer eBooks · doi:10.1007/978-4-431-56582-6_8 · Cited by 6 · see citing works
A minimally guided organoid model for cross-species comparisons of cerebellar developmentPreprint
Guglielmi, L., Sanchez, D. J. L.-D., González‐Martínez, J., & Lancaster, M. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.02.616236 · Cited by 4 · see citing works
Zebrin Expression in the Cerebellum of Two Crocodilian Species
Gutiérrez‐Ibáñez, C., Dannish, M. R., Kohl, T., Kettler, L., Carr, C. E., Tisdale, R. K., Iwaniuk, A. N., Luksch, H., & WYLIE, D. R. W. (2020) · Brain Behavior and Evolution · doi:10.1159/000505897 · Cited by 3 · see citing works
The Independent Evolution Method Is Not a Viable Phylogenetic Comparative Method
Griffin, R. H., & Yapuncich, G. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144147 · Cited by 2 · see citing works
Anatomie du cervelet et des voies cérébelleuses
Manto, M. U., & Habas, C. (2013) · Springer eBooks · doi:10.1007/978-2-8178-0447-7_2 · Cited by 2 · see citing works
Rickelton, K., Ely, J. J., Hopkins, W. D., Hof, P. R., Sherwood, C. C., Bauernfeind, A. L., & Babbitt, C. C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.03.641249 · Cited by 2 · see citing works
Cerebellar Purkinje cells change dendritic architecture during primate evolutionPreprint
Ferrell, A., Busch, S. E., Hillegas, M. E., Sherwood, C. C., & Hansel, C. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.07.728033 · Cited by 1 · see citing works
The Cerebro-Cerebellar Underpinning of Cognitive Control
Koziol, L. F. (2014) · SpringerBriefs in neuroscience · doi:10.1007/978-3-319-04477-4_15
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Clues to Understanding the Phylogeny of Behavioral Control
Koziol, L. F. (2014) · SpringerBriefs in neuroscience · doi:10.1007/978-3-319-04477-4_9
- Authors
- Smaers, J. B., Steele, J., & Zilles, K.
- Affiliations
- University College London (GB)
- Forschungszentrum Jülich (DE)
- Corresponding author
- Smaers, Jeroen B.
- Venue
- Annals of the New York Academy of Sciences
- Publisher
- Wiley
- Published
- 2011-04
- Volume
- 1225
- Issue
- 1
- Pages
- 176-190
- ISSN
- 0077-8923 (ISSN-L)
- 1749-6632
- OpenAlex
- W2172031244
- Cited by
- 50
- References
- 97
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 3 · 2017: 3 · 2016: 3 · 2015: 1 · 2014: 10 · 2013: 7 · 2012: 3
- FWCI
- 9.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of the New York Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- JuSER (Forschungszentrum Jülich) (submittedVersion)
- Funders
- Arts and Humanities Research Council (111956/1)
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Keywords
- primate brain evolution, anthropoid primates, functional specialization, evolutionary models, brain organization
- MeSH terms
- Anatomy, Comparative, Animals, Cerebellum, Cerebral Cortex, Biological Evolution, Humans, Models, Biological, Organ Specificity, Organ Size, Phylogeny, Primates, Species Specificity
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