Expansion of the neocerebellum in Hominoidea.

Technological and conceptual breakthroughs have led to more serious consideration of the cerebellum as an essential element in cognition. Recent studies show the lateral cerebellum, seat of the neocerebellum, to be most active in cognitive tasks. An examination of the relative volumes of the cerebellar hemispheres in anthropoids would reveal whether some groups show greater neocerebellar development through hemispheric expansion beyond expected allometry, implying a greater contribution of the lateral hemispheres to cognition. This study expands the existing data on primate brain and brain part volumes by incorporating data from both magnetic resonance scans and histological sections for a total sample size of 97 specimens, including 42 apes, 14 humans and 41 monkeys. The resulting volumes of whole brain, cerebellum, vermis, and hemisphere enable a reliable linear regression contrast between hominoids and monkeys, and demonstrate a striking increase in the lateral cerebellum in hominoids. The uniformity of the grade shift suggests that this increase took place in the common ancestor to the hominoids. The importance of the neocerebellum in visual-spatial skills, planning of complex movements, procedural learning, attention switching, and sensory discrimination in manipulation would facilitate the adaptation of these early hominoids to frugivory and suspensory feeding.

[1]  A. L. Leiner,et al.  The human cerebro-cerebellar system: its computing, cognitive, and language skills , 1991, Behavioural Brain Research.

[2]  R. Bauchot,et al.  ENCÉPHALISATION ET NIVEAU ÉVOLUTIF CHEZ LES SIMIENS , 1969 .

[3]  The cerebellum and its part in the evolution of the hominoid brain , 2000 .

[4]  J. Bower,et al.  Is the cerebellum sensory for motor's sake, or motor for sensory's sake: the view from the whiskers of a rat? , 1997, Progress in brain research.

[5]  A. Schleicher,et al.  The Cerebellum: An Asset to Hominoid Cognition , 2002 .

[6]  E. Courchesne,et al.  Attentional Activation of the Cerebellum Independent of Motor Involvement , 1997, Science.

[7]  D. Kleinbaum,et al.  Applied Regression Analysis and Other Multivariate Methods , 1978 .

[8]  J. Schmahmann An emerging concept. The cerebellar contribution to higher function. , 1991, Archives of neurology.

[9]  H. Damasio,et al.  The brain and its main anatomical subdivisions in living hominoids using magnetic resonance imaging. , 2000, Journal of human evolution.

[10]  T. Insel,et al.  Evolution of the Cerebellum in Primates: Differences in Relative Volume among Monkeys, Apes and Humans , 1998, Brain, Behavior and Evolution.

[11]  E Courchesne,et al.  Attention function and dysfunction in autism. , 2001, Frontiers in bioscience : a journal and virtual library.

[12]  A. L. Leiner,et al.  Reappraising the cerebellum: what does the hindbrain contribute to the forebrain? , 1989, Behavioral neuroscience.

[13]  R. Byrne The Thinking Ape : Evolutionary Origins of Intelligence , 1995 .

[14]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[15]  K. Milton Distribution Patterns of Tropical Plant Foods as an Evolutionary Stimulus to Primate Mental Development , 1981 .

[16]  Barbara J. King,et al.  The origins of language : what nonhuman primates can tell us , 1999 .

[17]  J. Schmahmann From movement to thought: Anatomic substrates of the cerebellar contribution to cognitive processing , 1996, Human brain mapping.

[18]  S. Matano A volumetric comparison of the vestibular nuclei in primates. , 1986, Folia primatologica; international journal of primatology.

[19]  K. Gibson,et al.  “Language” and intelligence in monkeys and apes: Comparative developmental perspectives on ape “language” , 1990 .

[20]  R. Barton Brain evolution (Communications arising): How did brains evolve? , 2002, Nature.

[21]  Damon A. Clark,et al.  Brain evolution (Communications arising): How did brains evolve? , 2002, Nature.

[22]  V. Howard,et al.  Unbiased Stereology: Three-Dimensional Measurement in Microscopy , 1998 .

[23]  G. Holmes THE CEREBELLUM OF MAN , 1939 .

[24]  B. Merker Silver staining of cell bodies by means of physical development , 1983, Journal of Neuroscience Methods.

[25]  L. Aiello Allometry and the analysis of size and shape in human evolution , 1992 .

[26]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.

[27]  T. Insel,et al.  The primate neocortex in comparative perspective using magnetic resonance imaging. , 1999, Journal of human evolution.

[28]  The cerebellum : from structure to control , 1997 .

[29]  M. Glickstein,et al.  Cerebellum and Neuronal Plasticity , 1987, NATO ASI Series.

[30]  P. Strick,et al.  Activation of a cerebellar output nucleus during cognitive processing. , 1994, Science.

[31]  W. T. Thach Motor Learning and Synaptic Plasticity in the Cerebellum: On the specific role of the cerebellum in motor learning and cognition: Clues from PET activation and lesion studies in man , 1997 .

[32]  P. Greenfield,et al.  Language, tools and brain: The ontogeny and phylogeny of hierarchically organized sequential behavior , 1991, Behavioral and Brain Sciences.

[33]  R. Bauchot,et al.  DONNEES NOUVELLES SUR L’ENCEPHALISATION DES INSECTIVORES ET DES PROSIMIENS , 1966 .

[34]  E. Courchesne,et al.  A new role for the cerebellum in cognitive operations. , 1992, Behavioral neuroscience.

[35]  S. Matano A Comparative Neuroprimatological Study on the Inferior Olivary Nuclei (from the STEPHAN's Collection) , 1992 .

[36]  Sue Taylor Parker,et al.  Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in cebus monkeys and great apes , 1977 .

[37]  K. Gibson,et al.  A developmental model for the evolution of language and intelligence in early hominids , 1979 .

[38]  H. D. Steklis Primate ecology and human origins: Edited by I. S. Bernstein and E. O. Smith. New York: Garland Press, 1980, 380 pp., $34.50 , 1981 .

[39]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[40]  R. Martin,et al.  Brain Size Allometry Ontogeny and Phylogeny , 1985 .

[41]  M. Tomasello,et al.  Joint attention and lexical acquisition style , 1983 .

[42]  C. Nunn,et al.  Comparative methods for studying primate adaptation and allometry , 2001 .

[43]  K. Gibson,et al.  “Language” and intelligence in monkeys and apes: New perspectives on instincts and intelligence: Brain size and the emergence of hierarchical mental constructional skills , 1990 .

[44]  A. L. Leiner,et al.  Does the cerebellum contribute to mental skills? , 1986, Behavioral neuroscience.

[45]  S. Larson Parallel evolution in the hominoid trunk and forelimb , 1998 .

[46]  Daniel J. Povinelli,et al.  Arboreal Clambering and the Evolution of Self-Conception , 1995, The Quarterly Review of Biology.

[47]  A. Schleicher,et al.  How many sections must be measured in order to reconstruct the volume of a structure using serial sections? , 1982, Microscopica acta.

[48]  E. Hirasaki,et al.  Volumetric comparisons in the cerebellar complex of anthropoids, with special reference to locomotor types. , 1997, American journal of physical anthropology.

[49]  Andrew Rambaut,et al.  Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data , 1995, Comput. Appl. Biosci..

[50]  William L. Jungers,et al.  Size and Scaling in Primate Biology , 1985, Advances in Primatology.

[51]  J. Jansen,et al.  Aspects of cerebellar anatomy , 1954 .

[52]  A. Purvis A composite estimate of primate phylogeny. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[53]  M. Tomasello,et al.  Joint attention and early language. , 1986, Child development.

[54]  J Townsend,et al.  Impairment in shifting attention in autistic and cerebellar patients. , 1994, Behavioral neuroscience.

[55]  H. Stephan,et al.  QUANTITATIVE COMPARATIVE NEUROANATOMY OF PRIMATES: AN ATTEMPT AT A PHYLOGENETIC INTERPRETATION * , 1969 .

[56]  A. L. Leiner,et al.  Cognitive and language functions of the human cerebellum , 1993, Trends in Neurosciences.

[57]  P. Rodman Primate Adaptation and Evolution, Second Edition , 2000 .

[58]  H. Stephan,et al.  Volume comparisons in the cerebellar complex of primates. I. Ventral pons. , 1985, Folia primatologica; international journal of primatology.

[59]  R. D. Martín,et al.  Adaptation and body size in primates. , 1980, Zeitschrift fur Morphologie und Anthropologie.

[60]  John G. Fleagle,et al.  Primate Adaptation and Evolution , 1989 .

[61]  J. F. Stein,et al.  Role of the cerebellum in the visual guidance of movement , 1986, Nature.

[62]  K. Gibson,et al.  Mammalian social learning : comparative and ecological perspectives , 1999 .

[63]  I. Bernstein Current problems in sociobiology Edited by Kings College Sociobiology Group. Cambridge University Press, Cambridge, 1982, 394 pp. Hardback: £27.50, ISBN 0-521-24203-7. Paperback: £9.95, ISBN 0-521-28250-8 , 1984, Behavioural Processes.

[64]  J. Bower,et al.  Cerebellum Implicated in Sensory Acquisition and Discrimination Rather Than Motor Control , 1996, Science.

[65]  Frahm Hd,et al.  Volume comparisons in the cerebellar complex of primates. II. Cerebellar nuclei. , 1985, Folia primatologica; international journal of primatology.

[66]  Partha P. Mitra,et al.  Scalable architecture in mammalian brains , 2001, Nature.

[67]  Phyllis C. Lee,et al.  Primate Ontogeny, Cognition and Social Behaviour , 1986 .