Electronic Theses and Dissertations Uc San Diego Title: Comparative Analysis of Broca's Area in Hominoids Comparative Analysis of Broca's Area in Hominoids

At the heart of the study of the evolution of language ability is the question how to produce testable hypotheses regarding the antecessors of language in our hominid ancestors and the presence or absence of such traits in our closest living relatives, the apes. One region that is consistently implicated in modern functional studies of language, and was implicated even in early lesion studies, is the region known as Broca's area (Brodmann's areas 44 and 45). The region's involvement in language function in humans is the reason that Broca's area is expected to express different anatomical characteristics from other prefrontal areas and to have unique characteristics in humans. In order to assess the degree to which the human brain has changed in relation to other hominoids, we need to have detailed knowledge, not only of the human brain, but also as many closely related species as possible. Previous studies have reported data on the comparative gross morphology of the inferior frontal gyrus, in which Broca's area is located in chimpanzees, bonobos, and gorillas (Cantalupo and Hopkins, 2001), but studies of the cytoarchitecture of Broca's area are limited to humans The purpose of this dissertation was to assess, both qualitatively and quantitatively, the cytoarchitectonic structure of Brodmann's areas 44 and 45 in human, chimpanzee, bonobo, gorilla, orangutan, and gibbon specimens. Quantitative measurements of minicolumnar organization, volume, neuron number, and neuron density revealed only limited differences between humans and apes. While volume of and neuronal number in Brodmann's areas 44 and 45 were larger in humans, neither were larger than expected. Furthermore, the relative size of the areas was not larger in humans than in apes and did not differentiate among ape species. Neuron density and grey level index (within minicolumns) were decreased in humans relative to apes, and only limited evidence for any asymmetry was observed. The variation among species in Brodmann's areas 44 and 45 eScholarship provides open access, scholarly publishing services to the University of California and delivers a dynamic research platform to scholars worldwide. suggests that this region behaves much as expected in response to changes in brain size. Despite Broca's area's involvement in language related behavior in humans, the current data provides no evidence that there are differences in information processing occurring in this region, and no pattern emerges that requires explanations other than those related to increases in brain size. This suggests Broca's area involvement in …

[1]  Manuel F. Casanova,et al.  Neocortical Modularity And The Cell Minicolumn , 2012 .

[2]  Katrin Amunts,et al.  A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca's area in humans and great apes , 2008, The Journal of comparative neurology.

[3]  Stephanie Clarke,et al.  Laminar specificity of intrinsic connections in Broca's area. , 2007, Cerebral cortex.

[4]  Nicole Barger,et al.  A comparative volumetric analysis of the amygdaloid complex and basolateral division in the human and ape brain. , 2007, American journal of physical anthropology.

[5]  A. Georgopoulos,et al.  Mapping of the preferred direction in the motor cortex , 2007, Proceedings of the National Academy of Sciences.

[6]  C. Fiebach,et al.  Dynamic Anticipatory Processing of Hierarchical Sequential Events: a Common Role for Broca's Area and Ventral Premotor Cortex Across Domains? , 2006, Cortex.

[7]  David Caplan,et al.  Why Is Broca'S Area Involved in Syntax? , 2006, Cortex.

[8]  Katrin Amunts,et al.  Left-Right Asymmetry in Volume and Number of Neurons in Adult Broca's Area , 2006, Cortex.

[9]  Luciano Fadiga,et al.  Hand Actions and Speech Representation in Broca's Area , 2006, Cortex.

[10]  Alex Martin,et al.  Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque , 2006, Nature Neuroscience.

[11]  D. Buxhoeveden,et al.  Microanatomy in 21 day rat brains exposed prenatally to cocaine , 2006, International Journal of Developmental Neuroscience.

[12]  E. Koechlin,et al.  Broca's Area and the Hierarchical Organization of Human Behavior , 2006, Neuron.

[13]  Conrado A. Bosman,et al.  The Origin of Broca’s Area and Its Connections from an Ancestral Working Memory Network , 2006 .

[14]  M. Petrides.  Broca’s Area in the Human and the Nonhuman Primate Brain , 2006 .

[15]  Matthias Schlesewsky,et al.  Processing linguistic complexity and grammaticality in the left frontal cortex. , 2005, Cerebral cortex.

[16]  W. Hopkins.  The Dynamic Dance: Nonvocal Communication in African Great Apes , 2005, International Journal of Primatology.

[17]  C. Sherwood,et al.  Primary motor cortex asymmetry is correlated with handedness in capuchin monkeys (Cebus apella). , 2005, Behavioral Neuroscience.

[18]  K. Semendeferi,et al.  Neural connectivity and cortical substrates of cognition in hominoids. , 2005, Journal of human evolution.

[19]  M. D. Neilson,et al.  Motor maps and synergies. , 2005, Human movement science.

[20]  P. Hagoort.  On Broca, brain, and binding: a new framework , 2005, Trends in Cognitive Sciences.

[21]  C. Sherwood,et al.  Is humanlike cytoarchitectural asymmetry present in another species with complex social vocalization? A stereologic analysis of mustached bat auditory cortex , 2005, Brain Research.

[22]  Su Li,et al.  Synchronized oscillation in a modular neural network composed of columns. , 2005, Science in China. Series C, Life sciences.

[23]  K. Amunts,et al.  Broca's region: from action to language. , 2005, Physiology.

[24]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[25]  A. Schleicher,et al.  Transmitter receptors and functional anatomy of the cerebral cortex , 2004, Journal of anatomy.

[26]  K. Rockland,et al.  Some thoughts on cortical minicolumns , 2004, Experimental Brain Research.

[27]  Peter Hagoort,et al.  Neural responses to the production and comprehension of syntax in identical utterances , 2004, Brain and Language.

[28]  Simon B. Eickhoff,et al.  Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—The roles of Brodmann areas 44 and 45 , 2004, NeuroImage.

[29]  R. Adolphs,et al.  Neural systems behind word and concept retrieval , 2004, Cognition.

[30]  Hernán D. Reisin,et al.  Interlaminar astroglia of the cerebral cortex: a marker of the primate brain , 2004, Brain Research.

[31]  Wenbo Xu,et al.  Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Jörg Lücke,et al.  Rapid Processing and Unsupervised Learning in a Model of the Cortical Macrocolumn , 2004, Neural Computation.

[33]  M. Nakamichi.  Tool-use and tool-making by captive, group-living orangutans (Pongo pygmaeus abelii) at an artificial termite mound , 2004, Behavioural Processes.

[34]  M. Mishkin,et al.  Species-specific calls evoke asymmetric activity in the monkey's temporal poles , 2004, Nature.

[35]  Timothy Edward John Behrens,et al.  Functional Asymmetry for Auditory Processing in Human Primary Auditory Cortex , 2003, The Journal of Neuroscience.

[36]  Katrin Amunts,et al.  Broca's region: Cytoarchitectonic asymmetry and developmental changes , 2003, The Journal of comparative neurology.

[37]  A. Georgopoulos,et al.  Modular organization of directionally tuned cells in the motor cortex: Is there a short-range order? , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[38]  S. Bookheimer,et al.  Dissociating Neural Mechanisms of Temporal Sequencing and Processing Phonemes , 2003, Neuron.

[39]  Patrick R Hof,et al.  Variability of Broca's area homologue in African great apes: implications for language evolution. , 2003, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[40]  R. E Passingham,et al.  Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study , 2003, NeuroImage.

[41]  Michelle Y. Merrill,et al.  Orangutan Cultures and the Evolution of Material Culture , 2003, Science.

[42]  A. Schleicher,et al.  Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry , 2002, European Neuropsychopharmacology.

[43]  K. Rockland,et al.  The pyramidal cell of the sensorimotor cortex of the macaque monkey: phenotypic variation. , 2002, Cerebral cortex.

[44]  R. Byrne,et al.  Leaf Processing by Wild Chimpanzees: Physically Defended Leaves Reveal Complex Manual Skills , 2002 .

[45]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[46]  D. Buxhoeveden,et al.  The minicolumn hypothesis in neuroscience. , 2002, Brain : a journal of neurology.

[47]  James K Rilling,et al.  A quantitative morphometric comparative analysis of the primate temporal lobe. , 2002, Journal of human evolution.

[48]  W. Hopkins,et al.  Asymmetric Broca's area in great apes , 2001, Nature.

[49]  R. Zatorre,et al.  Spectral and temporal processing in human auditory cortex. , 2001, Cerebral cortex.

[50]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[51]  Martha W. Burton,et al.  The role of inferior frontal cortex in phonological processing , 2001, Cogn. Sci..

[52]  Alan C. Evans,et al.  Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans. , 2001, Cerebral cortex.

[53]  M Litaker,et al.  Morphological differences between minicolumns in human and nonhuman primate cortex. , 2001, American journal of physical anthropology.

[54]  James B. Rowe,et al.  Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory , 2001, NeuroImage.

[55]  D. Buxhoeveden,et al.  Lateralization of Minicolumns in Human Planum temporale Is Absent in Nonhuman Primate Cortex , 2001, Brain, Behavior and Evolution.

[56]  R. Holloway,,et al.  Endocast of Sambungmacan 3 (Sm 3): A new Homo erectus from Indonesia , 2001, The Anatomical record.

[57]  D. Weinberger,et al.  Morphology of the Frontal Operculum: A Volumetric Magnetic Resonance Imaging Study of the Pars Triangularis , 2001, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[58]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[59]  D. V. von Cramon,et al.  Functional organization of the lateral premotor cortex: fMRI reveals different regions activated by anticipation of object properties, location and speed. , 2001, Brain research. Cognitive brain research.

[60]  Joseph Poulshock,et al.  Lingua ex Machina: Reconciling Darwin and Chomsky with the Human Brain , 2001 .

[61]  J. Raz,et al.  Contralateral monocular dominance in anterior visual cortex confirmed by functional magnetic resonance imaging. , 2000, American journal of ophthalmology.

[62]  C. Price.  The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

[63]  D. Buxhoeveden,et al.  Comparative lateralisation patterns in the language area of human, chimpanzee, and rhesus monkey brains , 2000, Laterality.

[64]  William M. Fields,et al.  Linguistic, Cultural and Cognitive Capacities of Bonobos(Pan Paniscus) , 2000 .

[65]  Jon H. Kaas,et al.  Why is Brain Size so Important:Design Problems and Solutions as Neocortex Gets Biggeror Smaller , 2000 .

[66]  Anthony R. Ives,et al.  Using the Past to Predict the Present: Confidence Intervals for Regression Equations in Phylogenetic Comparative Methods , 2000, The American Naturalist.

[67]  R. McCarley,et al.  Abnormal angular gyrus asymmetry in schizophrenia. , 2000, The American journal of psychiatry.

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

[69]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[70]  H. Uylings,et al.  Structural asymmetry of motor speech areas 44 and 45 in human cerebral cortex during postnatal ontogeny , 1999, Bulletin of Experimental Biology and Medicine.

[71]  B. Anderson,et al.  Anatomic asymmetries of the posterior superior temporal lobes: a postmortem study. , 1999, Neuropsychiatry, neuropsychology, and behavioral neurology.

[72]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[73]  Alan C. Evans,et al.  Morphology, morphometry and probability mapping of the pars opercularis of the inferior frontal gyrus: an in vivo MRI analysis , 1999, The European journal of neuroscience.

[74]  P. Goldman-Rakic,et al.  Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. , 1999, Journal of neurophysiology.

[75]  Anthony R. Ives,et al.  An Introduction to Phylogenetically Based Statistical Methods, with a New Method for Confidence Intervals on Ancestral Values , 1999 .

[76]  H. Gundersen,et al.  The efficiency of systematic sampling in stereology — reconsidered , 1999, Journal of microscopy.

[77]  P. Morosan,et al.  Observer-Independent Method for Microstructural Parcellation of Cerebral Cortex: A Quantitative Approach to Cytoarchitectonics , 1999, NeuroImage.

[78]  K Zilles,et al.  Limbic frontal cortex in hominoids: a comparative study of area 13. , 1998, American journal of physical anthropology.

[79]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[80]  G. Ehret,et al.  The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation , 1997, Journal of Comparative Physiology A.

[81]  Ikuo Taniguchi,et al.  The columnar and layer-specific response properties of neurons in the primary auditory cortex of Mongolian gerbils , 1997, Hearing Research.

[82]  Robin I. M. Dunbar.  Great Ape Societies , 1997 .

[83]  A. Schleicher,et al.  Structural Asymmetries in the Human Forebrain and the Forebrain of Non-human Primates and Rats , 1996, Neuroscience & Biobehavioral Reviews.

[84]  G. Rosen,et al.  Cellular, Morphometric, Ontogenetic and Connectional Substrates of Anatomical Asymmetry , 1996, Neuroscience & Biobehavioral Reviews.

[85]  T. L. Hayes,et al.  Magnopyramidal neurons in the anterior motor speech region. Dendritic features and interhemispheric comparisons. , 1996, Archives of neurology.

[86]  Alan C. Evans,et al.  Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. , 1996, Cerebral cortex.

[87]  N Suga,et al.  Facilitative responses to species-specific calls in cortical FM-FM neurons of the mustached bat. , 1996, Neuroreport.

[88]  P. Rakić,et al.  Numerical relationship between neurons in the lateral geniculate nucleus and primary visual cortex in macaque monkeys , 1996, Visual Neuroscience.

[89]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  P. Rakic.  Radial versus tangential migration of neuronal clones in the developing cerebral cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Mark Hallett,et al.  The role of reading activity on the modulation of motor cortical outputs to the reading hand in braille readers , 1995, Annals of neurology.

[92]  P. Rakic.  A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[93]  P S Goldman-Rakic,et al.  Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria. , 1995, Cerebral cortex.

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

[95]  J. A. Frost,et al.  Somatotopic mapping of the human primary motor cortex with functional magnetic resonance imaging , 1995, Neurology.

[96]  D. Kelly,et al.  Minicolumnar organization within somatosensory cortical segregates: I. Development of afferent connections. , 1994, Cerebral cortex.

[97]  Patrice Y. Simard,et al.  Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. , 1994, Cerebral cortex.

[98]  Tomoki Fukai,et al.  A model of cortical memory processing based on columnar organization , 1994, Biological Cybernetics.

[99]  B. Pakkenberg,et al.  Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors , 1993, Biological Psychiatry.

[100]  W. Bank.  The Human Brain. Surface, Three-Dimensional Sectional Anatomy and MRI , 1993 .

[101]  G. D. Rosen,et al.  Neuronal subtypes and anatomic asymmetry: changes in neuronal number and cell-packing density , 1993, Neuroscience.

[102]  R. Douglas,et al.  Exploring cortical microcircuits: a combined anatomical, physiological, and computational approach , 1992 .

[103]  B L Whitsel,et al.  Mechanisms underlying somatosensory cortical dynamics: II. In vitro studies. , 1992, Cerebral cortex.

[104]  G. Hewes.  Primate Communication and the Gestural Origin of Language , 1992, Current Anthropology.

[105]  H. Gundersen,et al.  Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator , 1991, The Anatomical record.

[106]  K. Kubota,et al.  Cytoarchitecture and intrafrontal connections of the frontal cortex of the brain of the hamadryas baboon (Papio hamadryas) , 1991, The Journal of comparative neurology.

[107]  P. Goldman-Rakic,et al.  Myelo‐ and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[108]  G. Ojemann.  Cortical organization of language , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  A. Peters,et al.  Organization of pyramidal neurons in area 17 of monkey visual cortex , 1991, The Journal of comparative neurology.

[110]  Francine G. P. Patterson,et al.  Language acquisition by a lowland gorilla: Koko's first ten years of vocabulary development , 1990 .

[111]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[112]  T. Deacon.  Problems of ontogeny and phylogeny in brain-size evolution , 1990, International Journal of Primatology.

[113]  K Zilles,et al.  A quantitative approach to cytoarchitectonics: Analysis of structural inhomogeneities in nervous tissue using an image analyser , 1990, Journal of microscopy.

[114]  M. Hofman.  On the evolution and geometry of the brain in mammals , 1989, Progress in Neurobiology.

[115]  D. Pandya,et al.  Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey , 1989, The Journal of comparative neurology.

[116]  M. Posner,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[117]  H. J. G. GUNDERSEN,et al.  Some new, simple and efficient stereological methods and their use in pathological research and diagnosis , 1988, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[118]  H Haug,et al.  Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). , 1987, The American journal of anatomy.

[119]  A. Peters,et al.  The neuronal composition of area 17 of rat visual cortex. IV. The organization of pyramidal cells , 1987, The Journal of comparative neurology.

[120]  D. Pandya,et al.  Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey , 1987, The Journal of comparative neurology.

[121]  G. Murphy,et al.  Volumetric asymmetry in the human striate cortex , 1985, Experimental Neurology.

[122]  I. Fried,et al.  Dendritic organization of the anterior speech area , 1985, Experimental Neurology.

[123]  William C. Stebbins,et al.  Neural lateralization of vocalizations by Japanese macaques: communicative significance is more important than acoustic structure. , 1984, Behavioral neuroscience.

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

[125]  D. Falk.  Cerebral Cortices of East African Early Hominids , 1983, Science.

[126]  H. Kretschmann,et al.  Different volume changes of cerebral cortex and white matter during histological preparation. , 1982, Microscopica acta.

[127]  H. Seldon.  Structure of human auditory cortex. I. Cytoarchitectonics and dendritic distributions , 1981, Brain Research.

[128]  R. Passingham,et al.  Broca's area and the origins of human vocal skill. , 1981, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[129]  J A Wada,et al.  Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adults and 100 infant brains. , 1975, Archives of neurology.

[130]  R. Gardner,et al.  Teaching sign language to a chimpanzee. , 1969, Science.

[131]  R. Holloway,.  The evolution of the primate brain: some aspects of quantitative relations. , 1968, Brain research.

[132]  J. Kernohan.  The Organization of the Cerebral Cortex , 1957 .

[133]  A. Walker,et al.  A cytoarchitectural study of the prefrontal area of the macaque monkey , 1940 .

[134]  Kevin Fiedler,et al.  Grooming Gossip And The Evolution Of Language , 2016 .

[135]  D. Fragaszy,et al.  Tool use and cognition in primates , 2010 .

[136]  Anders Lansner,et al.  Non-commercial Research and Educational Use including without Limitation Use in Instruction at Your Institution, Sending It to Specific Colleagues That You Know, and Providing a Copy to Your Institution's Administrator. All Other Uses, Reproduction and Distribution, including without Limitation Comm , 2022 .

[137]  P. Goldman-Rakic,et al.  Regional specificity in the neuropathologic substrates of schizophrenia: a morphometric analysis of Broca's area 44 and area 9. , 2003, Archives of general psychiatry.

[138]  S. Bookheimer.  Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[139]  B. Keverne,et al.  Book Review: Evolutionary Anatomy of the Primate Cerebral Cortex. Edited by Dean Falk and Kathleen R. Gibson, Cambridge University Press, Cambridge, MA, 2001, xvii + 344 pp., $80.00 (hardback) , 2002, International Journal of Primatology.

[140]  Richard W. Byrne,et al.  ESTIMATING THE COMPLEXITY OF ANIMAL BEHAVIOUR: HOW MOUNTAIN GORILLAS EAT THISTLES , 2001 .

[141]  A. Whiten,et al.  CHARTING CULTURAL VARIATION IN CHIMPANZEES , 2001 .

[142]  Laure Zago,et al.  Mental calculation in a prodigy is sustained by right prefrontal and medial temporal areas , 2001, Nature Neuroscience.

[143]  L. White,et al.  Structure of the human sensorimotor system. I: Morphology and cytoarchitecture of the central sulcus. , 1997, Cerebral cortex.

[144]  L. White,et al.  Structure of the human sensorimotor system. II: Lateral symmetry. , 1997, Cerebral cortex.

[145]  Sherman Wilcox,et al.  Gesture and the Nature of Language , 1995 .

[146]  M. Petrides.  Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[147]  J L Ringo,et al.  Neuronal interconnection as a function of brain size. , 1991, Brain, behavior and evolution.

[148]  K. Brodmann.  Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[149]  F. Gallyas,et al.  A principle for silver staining of tissue elements by physical development. , 1971, Acta morphologica Academiae Scientiarum Hungaricae.

[150]  Warren S. McCulloch,et al.  The isocortex of the chimpanzee. , 1950 .

[151]  C. J. Connolly,et al.  External morphology of the primate brain , 1950 .

[152]  P. Broca,et al.  Remarques sur le siege de la faculte du langage articule suivies d'une observation d'aphemie , 1861 .

[153]  V. Mountcastle.  REVIEW ARTICLE The , 2004 .