Modeling the evolution of cortico-cerebellar systems in primates
Jeroen B. Smaers
University College London, Institute of Archaeology, AHRC Centre for the Evolution of Cultural Diversity, London, UK.
Search for more papers by this authorJames Steele
University College London, Institute of Archaeology, AHRC Centre for the Evolution of Cultural Diversity, London, UK.
Search for more papers by this authorKarl Zilles
Institute of Neuroscience and Medicine INM-2, Research Centre Jülich, Jülich, Germany.
C. & O. Vogt Institute of Brain Research, University of Düsseldorf, Düsseldorf, Germany
Search for more papers by this authorJeroen B. Smaers
University College London, Institute of Archaeology, AHRC Centre for the Evolution of Cultural Diversity, London, UK.
Search for more papers by this authorJames Steele
University College London, Institute of Archaeology, AHRC Centre for the Evolution of Cultural Diversity, London, UK.
Search for more papers by this authorKarl Zilles
Institute of Neuroscience and Medicine INM-2, Research Centre Jülich, Jülich, Germany.
C. & O. Vogt Institute of Brain Research, University of Düsseldorf, Düsseldorf, Germany
Search for more papers by this authorAbstract
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.
References
- 1 Jerison, H.J. 1973. Evolution of the Brain and Intelligence. Academic Press. New York .
- 2 Carreiras, M. et al. 2009. An anatomical signature for literacy. Nature 461: 983–986.
- 3 Draganski, B. et al. 2004. Changes in grey matter induced by training. Nature 427: 311–312.
- 4 Fleming, S.M. et al. 2010. Relating introspective accuracy to individual differences in brain structure. Science 329: 1541–1543.
- 5 Scholz, J. et al. 2009. Training induces changes in white-matter architecture. Nat. Neurosci. 12: 1370–1371.
- 6 Huber, R. et al. 1997. Microhabitat use, trophic patterns, and the evolution of brain structure in african cichlids. Brain. Behav. Evol. 50: 167–182.
- 7 Iwaniuk, A.N. & D.R.W. Wylie. 2007. Neural specialization for hovering in hummingbirds: hypertrophy of the pretectal nucleus lentiformis mesencephali. J. Comp. Neurol. 500: 211–221.
- 8 Smith, A R. et al. 2010. Socially induced brain development in a facultatively eusocial sweat bee Megalopta genalis (Halictidae). Proc. R. Soc. B Biol. Sci. 277: 2157–2163.
- 9 Dunbar, R.I.M. & S. Shultz. 2007. Evolution in the social brain. Science 317: 1344–1347.
- 10 Welker, W. & S. Seidenstein. 1958. External morphology of the cerebral cortex of the raccoon (Procyon lotor) in relation to development of sensory receiving areas. Anat. Rec. 130: 387–388.
- 11 Barton, R.A., A. Purvis & P.H. Harvey. 1995. Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 348: 381–392.
- 12 Barton, R.A. & P.H. Harvey. 2000. Mosaic evolution of brain structure in mammals. Nature 405: 1055–1058.
- 13 Whiting, B.A. & R.A. Barton. 2003. The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. J. Hum. Evol. 44: 3–10.
- 14 Barton, R.A. 2007. Evolutionary specialization in mammalian cortical structure. J. Evol. Biol. 20: 1504–1511.
- 15 Rilling, J.K. 2006. Human and nonhuman primate brains: Are they allometrically scaled versions of the same design? Evol. Anthropol. 15: 65–77.
- 16 Byrne, R.W. & N. Corp. 2004. Neocortex size predicts deception rate in primates. Proc. R. Soc. London, Ser. B Biol. Sci. 271: 1693–1699.
- 17 de Winter, W. & C.E. Oxnard. 2001. Evolutionary radiations and convergences in the structural organization of the mammalian brain. Nature 409: 710–714.
- 18 Schmahmann, J.D. & D.N. Pandya. 1997. The cerebrocerebellar system. In The Cerebellum and Cognition. J. D. Schmahmann, Ed.: 31–60. Academic Press. San Diego .
- 19 Stoodley, C.J. & J.D. Schmahmann. 2009. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44: 489–501.
- 20 Ramnani, N. 2006. The primate cortico-cerebellar system: anatomy and function. Nat. Rev. Neurosci. 7: 511–522.
- 21 Barton, R.A. 2007. Evolution of the social brain as a distributed neural system. In Oxford Handbook of Evolutionary Psychology. R.I.M. Dunbar & L. Barrett, Eds.: 129–144. Oxford University Press. New York .
- 22 Herculano-Houzel, S. 2010. Coordinated scaling of cortical and cerebellar numbers of neurons. Front. Neuroanat. 4: 1–8.
- 23 Ramnani, N. et al. 2006. The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from macaque monkeys and humans. Cereb. Cortex 16: 811–818.
- 24 Balsters, J.H. et al. 2010. Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules. Neuroimage 49(3): 2045–2052.
- 25 Krienen, F.M. & R.L. Buckner. 2009. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb. Cortex 19: 2485–2497.
- 26 Middleton, F.A. & P.L. Strick. 2000. Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain. Cogn. 42: 183–200.
- 27 Middleton, F.A. & P.L. Strick. 2000. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res. Rev. 31: 236–250.
- 28 Doyon, J., V. Penhune & L.G. Ungerleider. 2003. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41: 252–262.
- 29 Salmi, J. et al. 2010. Cognitive and motor loops of the human cerebra-cerebellar system. J. Cogn. Neurosci. 22: 2663–2676.
- 30 Voogd, J. & M. Glickstein. 1998. The anatomy of the cerebellum. Trends Neurosci. 21: 370–375.
- 31 Smaers, J.B. et al. 2010. Frontal white matter volume is associated with brain enlargement and higher structural connectivity in haplorrhine primates. PLoS One. 5: E9123: 1–6.
- 32 Smaers, J.B. & L. Vinicius. 2009. Inferring macro-evolutionary patterns using an adaptive peak model of evolution. Evol. Ecol. Res. 11: 991–1015.
- 33 Zilles, K., K. Amunts & J.B. Smaers. 2011. Three brain collections for comparative neuroanatomy and neuroimaging. Ann. N.Y. Acad. Sci. 1225(S1): in press.
- 34 Brodal, A. 1981. The cerebellum. In Neurological Anatomy in Relation to Clinical Medicine: 294–393. Oxford University Press. Oxford .
- 35 Glickstein, M., F. Sultan & J. Voogd. 2011. Functional localization in the cerebellum. Cortex 47: 59–80.
- 36 Marr, D. 1969. A theory of cerebellar cortex. J. Physiol. Lond. 202: 437–470.
- 37 Albus, J.S. 1971. A theory of cerebellar function. Math. Biosci. 10: 25–61.
10.1016/0025-5564(71)90051-4 Google Scholar
- 38 Middleton, F. A. & P. L. Strick. 1997. Cerebellar output channels. Cerebellum Cogn. 41: 61–82.
- 39 Brodal, A. 1992. The Central Nervous System: Structure and Function. Oxford University Press. Oxford .
- 40 Martin, J.H. 1996. The cerebellum. In Neuroanatomy: Text and Atlas: 291–322. Appleton & Lange. Stamford , CT .
- 41 Strick, P. L. 1983. The influence of motor preparation on the response of cerebellar neurons to limb displacements. J. Neurosci. 3: 2007–2020.
- 42 Blakemore, S.J. & A. Sirigu. 2003. Action prediction in the cerebellum and in the parietal lobe. Exp. Brain Res. 153: 239–245.
- 43 Bastian, A.J. 2006. Learning to predict the future: the cerebellum adapts feedforward movement control. Curr. Opin. Neurobiol. 16: 645–649.
- 44 Naito, E. et al. 2002. Internally simulated movement sensations during motor imagery activate cortical motor areas and the cerebellum. J. Neurosci. 22: 3683–3691.
- 45 Lang, C.E. & A.J. Bastian. 1999. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J. Neurophysiol. 82: 2108–2119.
- 46 Diedrichsen, J. et al. 2005. Neural correlates of reach errors. J. Neurosci. 25: 9919–9931.
- 47 Maschke, M. et al. 2004. Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J. Neurophysiol. 91: 230–238.
- 48 Smith, M.A. & R. Shadmehr. 2005. Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. J. Neurophysiol. 93: 2809–2821.
- 49 Stoodley, C.J. & J.D. Schmahmann. 2009. The cerebellum and language: evidence from patients with cerebellar degeneration. Brain Lang. 110: 149–153.
- 50 Raichle, M.E. et al. 1994. Practice related changes in human brain functional anatomy during nonmotor learning. Cereb. Cortex 4: 8–26.
- 51 MacLeod, C.E. et al. 2003. Expansion of the neocerebellum in Hominoidea. J. Hum. Evol. 44: 401–429.
- 52 Cavalieri, B. 1635. Geometria degli Indivisibili. Unione Tipografico-Editrice Torinese. Torino.
- 53 Howard, C.V. & M.G. Reed. 1998. Unbiased stereology. Three-Dimensional Measurement in Microscopy: 53–65. Springer-Verlag. New York .
- 54 Zilles, K., A. Schleicher & F.W. Pehlemann. 1982. How many sections must be measured in order to reconstruct the volume of a structure using serial sections? Microsc. Acta 86: 339–346.
- 55 Stephan, H., H. Frahm & G. Baron. 1981. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol. (Basel) 35: 1–29.
- 56 Matano, S. et al. 1985. Volume comparisons in the cerebellar complex of primates: 2. Cerbellar nuclei. Folia Primatol. (Basel) 44: 182–203.
- 57 Matano, S. 1986. A volumetric comparison of the vestibular nuclei in primates. Folia Primatol. (Basel) 47: 189–203.
- 58 Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125: 1–15.
- 59 Felsenstein, J. 1988. Phylogenies and quantitative characters. Annu. Rev. Ecol. Syst. 19: 445–471.
- 60 Martins, E.P. & T.F. Hansen. 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149: 646–667.
- 61 Smith, R.J. & J.M. Cheverud. 2002. Scaling of sexual dimorphism in body mass: a phylogenetic analysis of Rensch's rule in primates. Int. Am. J. Primatol. 23: UNSP 0164-0291/02/1000-1095/0.
- 62 Purvis, A. 1995. A composite estimate of primate phylogeny. Philos. Trans. R. Soc. London, Ser. B Biol Sci. 348: 405–421.
- 63 Martins, E.P. 2004. COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Distributed by the author at http://compare.bio.indiana.edu/.
- 64 Fleagle, J.G. 1999. Primate adaptation and evolution. Academic Press. New York .
- 65 Westoby, M., M.R. Leishman & J.M. Lord. 1995. On misinterpreting the phylogenetic correction. J. Ecol. 83: 531–534.
- 66 Price, T. 1997. Correlated evolution and independent contrasts. Philos. Trans. R. Soc. London, Ser. B Biol. Sci. 352: 519–529.
- 67 Harvey, P. H. & M.D. Pagel. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press. Oxford.
10.1093/oso/9780198546412.001.0001 Google Scholar
- 68 Harvey, P. H. & A. Rambaut. 2000. Comparative analyses for adaptive radiations. Philos. Trans. R. Soc. London, Ser. B Biol. Sci. 355: 1599–1605.
- 69 Butler, M.A. & A.A. King. 2004. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am. Nat. 164: 683–695.
- 70 Hansen, T.F. & S.H. Orzack. 2005. Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons. Evolution 59: 2063–2072.
- 71 Martins, E.P., J.A.F. Diniz & E.A. Housworth. 2002. Adaptive constraints and the phylogenetic comparative method: a computer simulation test. Evolution 56: 1–13.
- 72 Middleton, F.A. & P.L. Strick. 2001. Cerebellar projections to the prefrontal cortex of the primate. J. Neurosci. 21: 700–712.
- 73 Middleton, F.A. & P.L. Strick. 2002. Basal-ganglia ‘projections’ to the prefrontal cortex of the primate. Cereb. Cortex 12: 926–935.
- 74 Ramayya, A.G., M.F. Glasser & J.K. Rilling. 2010. A DTI investigation of neural substrates supporting tool use. Cereb. Cortex 20: 507–516.
- 75 Semendeferi, K. et al. 2002. Humans and great apes share a large frontal cortex. Nat. Neurosci. 5: 272–276.
- 76 Dunbar, R.I.M. & S. Shultz. 2007. Understanding primate brain evolution. Philos. Trans. R. Soc. B Biol. Sci. 362: 649–658.
- 77 Matano, S. & E. Hirasaki. 1997. Volumetric comparisons in the cerebellar complex of anthropoids, with special reference to locomotor types. Am. J. Phys. Anthropol. 103: 173–183.
10.1002/(SICI)1096-8644(199706)103:2<173::AID-AJPA4>3.0.CO;2-V CASPubMedWeb of Science®Google Scholar
- 78 Napier, J.R. & P. H. Napier. 1985. The Natural History of the Primates. The British Museum (Natural History). London .
- 79 Picard, N. & P.L. Strick. 1996. Motor areas of the medial wall: a review of their location and functional activation. Cereb. Cortex 6: 342–353.
- 80 Tanji, J. 1996. New concepts of the supplementary motor area. Curr. Opin. Neurobiol. 6: 782–787.
- 81 Campbell, C.J. et al. 2007. Primates in Perspective. Oxford University Press, New York .
- 82 Whiten, A. et al. 1999. Cultures in chimpanzees. Nature 399: 682–685.
- 83 Whiten, A. 2005. The second inheritance system of chimpanzees and humans. Nature 437: 52–55.
- 84 Whiten, A., V. Horner & F.B.M. de Waal. 2005. Conformity to cultural norms of tool use in chimpanzees. Nature 437: 737–740.
- 85 Biro, D. et al. 2003. Cultural innovation and transmission of tool use in wild chimpanzees: evidence from field experiments. Anim. Cogn. 6: 213–223.
- 86 Nagell, K., R.S. Olguin & M. Tomasello. 1993. Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). J. Comp. Psychol. 107: 174–186.
- 87 McGrew, W.C. 2010. Chimpanzee technology. Science 328: 579–580.
- 88 Call, J. & M. Tomasello. 1994. The social learning of tool use by orangutans (Pongo pygmaeus). J. Hum. Evol. 9: 297–313.
10.1007/BF02435516 Google Scholar
- 89 Breuer, T., M. Ndoundou-Hockemba & V. Fishlock. 2005. First observation of tool use in wild gorillas. Plos Biol. 3: 2041–2043.
- 90 van Schaik, C.P. et al. 2003. Orangutan cultures and the evolution of material culture. Science 299: 102–105.
- 91 Byrne, R.W. 2007. Culture in great apes: using intricate complexity in feeding skills to trace the evolutionary origin of human technical prowess. Philos. Trans. R. Soc. B Biol. Sci. 362: 577–585.
- 92 Fontaine, B., P.Y. Moisson & E.J. Wickings. 1995. Observations of spontaneous tool making and tool use in a captive group of western lowland gorillas (Gorilla gorilla gorilla). Folia Primatol. (Basel) 65: 219–223.
- 93 Roth, G. & U. Dicke. 2005. Evolution of the brain and intelligence. Trends Cogn. Sci. 9: 250–257.
- 94 Smaers, J.B. et al. Primate prefrontal cortex evolution: human brains are the extreme of a lateralized ape trend. Brain Behav. Evol. In Press. doi:10.1159/000323671.
- 95 Adolphs, R. 2009. The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 60: 693–716.
- 96 Pawlowski, B., C.B. Lowen & R.I. M. Dunbar. 1998. Neocortex size, social skills and mating success in primates. Behaviour 135: 357–368.
- 97 Kudo, H. & R. I. M. Dunbar. 2001. Neocortex size and social network size in primates. Anim. Behav. 62: 711–722.
- 98 DeVoogd, T. et al. 1993. Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses among oscine birds. Proc. R. Soc. B Biol. Sci. 254: 75–82.
- 99 Dunbar, R.I.M. 1992. Neocortex size as a constraint on group-size in primates. J. Hum. Evol. 22: 469–493.