The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution
Abstract
Investigations into the evolution of the primate brain have tended to neglect the role of connectivity in determining which brain structures have changed in size, focusing instead on changes in the size of the whole brain or of individual brain structures, such as the neocortex, in isolation. We show that the primate cerebellum, neocortex, vestibular nuclei and relays between them exhibit correlated volumetric evolution, even after removing the effects of change in other structures. The patterns of correlated evolution among individual nuclei correspond to their known patterns of connectivity. These results support the idea that the brain evolved by mosaic size change in arrays of functionally connected structures. Furthermore, they suggest that the much discussed expansion of the primate neocortex should be re-evaluated in the light of conjoint cerebellar expansion.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
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 [67]
Cites
Phylogenies and the Comparative Method
Felsenstein, J. (1985) · The American Naturalist · doi:10.1086/284325 · Cited by 9,793 · see citing works
The comparative method in evolutionary biology
Harvey, P., & Pagel, M. (1991) · Choice Reviews Online · doi:10.5860/choice.29-5104 · Cited by 4,778 · see citing works
(2005) · Choice Reviews Online · doi:10.5860/choice.43-0626 · Cited by 4,726 · see citing works
Neocortex size as a constraint on group size in primates
Dunbar, R. I. M. (1992) · Journal of Human Evolution · doi:10.1016/0047-2484(92)90081-j · Cited by 2,542 · see citing works
(1995) · Choice Reviews Online · doi:10.5860/choice.32-5931 · Cited by 2,337 · see citing works
Information processing in the primate visual system: an integrated systems perspective
Van Essen, D. C., Anderson, C. H., & Felleman, D. J. (1992) · Science · doi:10.1126/science.1734518 · Cited by 1,266 · 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
Purvis, A., & Rambaut, A. (1995) · Computer applications in the biosciences · doi:10.1093/bioinformatics/11.3.247 · Cited by 1,126 · see citing works
Cerebellar Projections to the Prefrontal Cortex of the Primate
Middleton, F. A., & Strick, P. L. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-02-00700.2001 · Cited by 1,034 · see citing works
New and Revised Data on Volumes of Brain Structures in Insectivores and Primates
Stephan, H., Frahm, H. D., & Baron, G. (1981) · Folia Primatologica · doi:10.1159/000155963 · Cited by 878 · see citing works
Mosaic evolution of brain structure in mammals
Barton, R. A., & Harvey, P. H. (2000) · Nature · doi:10.1038/35016580 · Cited by 797 · see citing works
Self-citationCognitive and language functions of the human cerebellum
Leiner, H. C., Leiner, A. L., & Dow, R. S. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90072-t · Cited by 753 · see citing works
IMPAIRED NON-MOTOR LEARNING AND ERROR DETECTION ASSOCIATED WITH CEREBELLAR DAMAGE
Fiez, J. A., Petersen, S. E., Cheney, M. K., & Raichle, M. E. (1992) · Brain · doi:10.1093/brain/115.1.155 · Cited by 630 · see citing works
Machiavellian Intelligence II: Extensions and Evaluations
(1997) · doi:10.1017/cbo9780511525636 · Cited by 514 · see citing works
Jacob, F. (1982) · DigitalGeorgetown (Georgetown University Library) · Cited by 365 · see citing works
Dunbar, R. (2003) · Science · doi:10.1126/science.1092116 · Cited by 314 · 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
Bearder, S. K., & Passingham, R. E. (1983) · Man · doi:10.2307/2801447 · Cited by 227 · see citing works
Analysis of Connectivity: Neural Systems in the Cerebral Cortex
Young, M. P., Scanneil, J. W., Burns, G., & Blakemore, C. B. (1994) · Reviews in the Neurosciences · doi:10.1515/revneuro.1994.5.3.227 · Cited by 189 · see citing works
Fallacies of progression in theories of brain-size evolution
Deacon, T. W. (1990) · International Journal of Primatology · doi:10.1007/bf02192869 · Cited by 158 · see citing works
The meaning of evolution, a study of the history of life and of its significance for man.
Simpson, G. G. (1949) · Yale University Press eBooks · doi:10.5962/bhl.title.40704 · Cited by 153 · see citing works
Rilling, J. K., & Insel, T. R. (1998) · Brain, Behavior and Evolution · doi:10.1159/000006575 · Cited by 131 · see citing works
Language impairments in patients with cerebellar lesions
Fabbro, F., Moretti, R., & Bava, A. (2000) · Journal of Neurolinguistics · doi:10.1016/s0911-6044(00)00010-5 · Cited by 130 · see citing works
Volume Comparisons in the Cerebellar Complex of Primates
Matano, S., Baron, G., Stephan, H., & Frahm, H. D. (1985) · Folia Primatologica · doi:10.1159/000156212 · Cited by 49 · see citing works
Matano, S., & Hirasaki, E. (1997) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(199706)103:2 · Cited by 36 · see citing works
Volume Comparisons in the Cerebellar Complex of Primates
Matano, S., Stephan, H., & Baron, G. (1985) · Folia Primatologica · doi:10.1159/000156211 · Cited by 30 · see citing works
Barton, R. A. (2002) · Nature · doi:10.1038/415134a · Cited by 28 · see citing works
Self-citationA Volumetric Comparison of the Vestibular Nuclei in Primates
Matano, S. (1986) · Folia Primatologica · doi:10.1159/000156277 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The human brain in numbers: a linearly scaled-up primate brain
Herculano-Houzel, S. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.031.2009 · Cited by 1,778 · see citing works
“A reasonable approximation was provided by Williams and Herrup (1988), from the compilation of partial numbers in the literature.”
Stoodley, C. J., & Schmahmann, J. D. (2010) · Cortex · doi:10.1016/j.cortex.2009.11.008 · Cited by 1,360 · see citing works
Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity
Krienen, F. M., & Buckner, R. L. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp135 · Cited by 782 · see citing works
Herculano-Houzel, S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201895109 · Cited by 726 · see citing works
The Cerebellum and Cognition: Evidence from Functional Imaging Studies
Stoodley, C. J. (2012) · The Cerebellum · doi:10.1007/s12311-011-0260-7 · Cited by 686 · see citing works
A critique of comparative studies of brain size
Healy, S. D., & Rowe, C. (2007) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2006.3748 · Cited by 528 · see citing works
Rapid evolution of the cerebellum in humans and other great apes
Barton, R. A., & Venditti, C. (2014) · Current Biology · doi:10.1016/j.cub.2014.08.056 · Cited by 291 · see citing works
Self-citationCoordinated scaling of cortical and cerebellar numbers of neurons
Herculano-Houzel (2010) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2010.00012 · Cited by 288 · see citing works
Balsters, J. H., Cussans, E., Diedrichsen, J., Phillips, K. A., Preuss, T. M., Rilling, J. K., & Ramnani, N. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.045 · Cited by 241 · see citing works
Embodied cognitive evolution and the cerebellum
Barton, R. A. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0112 · Cited by 210 · see citing works
Self-citationThe Evolution of Cerebrotypes in Birds
Iwaniuk, A. N., & Hurd, P. L. (2005) · Brain, Behavior and Evolution · doi:10.1159/000084313 · Cited by 205 · see citing works
Primate cognition: from ‘what now?’ to ‘what if
Barrett, L. (2003) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2003.09.005 · Cited by 169 · see citing works
Cerebellar volume and cognitive functioning in children who experienced early deprivation
Bauer, P. M., Hanson, J. L., Pierson, R. K., Davidson, R. J., & Pollak, S. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.014 · Cited by 167 · see citing works
Brains matter, bodies maybe not: the case for examining neuron numbers irrespective of body size
Herculano‐Houzel, S. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.05976.x · Cited by 137 · see citing works
Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution
Smaers, J. B., & Soligo, C. (2013) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2013.0269 · Cited by 112 · see citing works
Primate brain architecture and selection in relation to sex
Lindenfors, P., Nunn, C. L., & Barton, R. A. (2007) · BMC Biology · doi:10.1186/1741-7007-5-20 · Cited by 86 · see citing works
Self-citationSmaers, J. B., Schleicher, A., Zilles, K., & Vinicius, L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009123 · Cited by 81 · see citing works
Quantitative uniqueness of human brain evolution revealed through phylogenetic comparative analysis
Miller, I. F., Barton, R. A., & Nunn, C. L. (2019) · eLife · doi:10.7554/elife.41250 · Cited by 70 · see citing works
Self-citationModeling the evolution of cortico‐cerebellar systems in primates
Smaers, J. B., Steele, J., & Zilles, K. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06003.x · Cited by 50 · see citing works
Wartel, A., Lindenfors, P., & Lind, J. (2019) · PLOS ONE · doi:10.1371/journal.pone.0218655 · Cited by 40 · see citing works
Lefebvre, L. (2012) · Progress in Brain Research · doi:10.1016/b978-0-444-53860-4.00019-2 · Cited by 36 · see citing works
Understanding the Evolution of Mammalian Brain Structures; the Need for a (New) Cerebrotype Approach
Willemet, R. (2012) · Brain Sciences · doi:10.3390/brainsci2020203 · Cited by 25 · see citing works
- Authors
- Whiting, B. A., & Barton, R. A.
- Affiliations
- Durham University (GB)
- Corresponding author
- Whiting, B.A
- ORCID
- Barton, R.A
- Venue
- Journal of Human Evolution
- Publisher
- Elsevier BV
- Published
- 2003-01
- Volume
- 44
- Issue
- 1
- Pages
- 3-10
- ISSN
- 0047-2484 (ISSN-L)
- OpenAlex
- W1999446466
- Cited by
- 137
- References
- 28
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 8 · 2023: 3 · 2022: 4 · 2021: 9 · 2020: 2 · 2019: 11 · 2018: 8 · 2017: 8 · 2016: 7 · 2015: 2 · 2014: 6 · 2013: 5 · 2012: 17
- FWCI
- 5.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Human Evolution (publishedVersion)
- PubMed (publishedVersion)
- Durham Research Online (Durham University) (acceptedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Physical Sciences › Mathematics › Geometry and Topology › Morphological variations and asymmetry
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- primate brain evolution, cerebellum, neocortex, vestibular nuclei, brain connectivity, brain size
- MeSH terms
- Anatomy, Comparative, Animals, Anthropometry, Cerebellar Cortex, Biological Evolution, Pons, Primates, Thalamus, Vestibular Nuclei, Neocortex
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