Neural connectivity and cortical substrates of cognition in hominoids.

Cognitive functions and information processing recruit discrete neural systems in the cortex and white matter. We tested the idea that specific regions in the cerebrum are differentially enlarged in humans and that some of the neural reorganizational events that took place during hominoid evolution were species-specific and independent of changes in absolute brain size. We used magnetic resonance images of the living brains of 10 human and 17 ape subjects to obtain volumetric estimates of regions of interest. We parcellated the white matter in the frontal and temporal lobes into two sectors, including the white matter immediately underlying the cortex (gyral white matter) and the rest of white matter (core). We outlined the dorsal, mesial, and orbital subdivisions of the frontal lobe and analyzed the relationship between cortex and gyral white matter within each subdivision. For all regions analyzed, the observed human values are as large as expected, with the exception of the gyral white matter, which is larger than expected in humans. We found that orangutans had a relatively smaller orbital sector than any other great ape species, with no overlap in individual values. We found that the relative size of the dorsal subdivision is larger in chimpanzees than in bonobos, and that the ratio of gyral white matter to cortex stands out in Pan in comparison to Gorilla and Pongo. Individual variability, possible sex differences, and hemispheric asymmetries were present not only in humans, but in apes as well. Differences in the distribution of neural connectivity and cortical sectors were identified among great ape species that share similar absolute brain sizes. Given that these regions are part of neural systems with distinct functional attributes, we suggest that the observed differences may reflect different evolutionary pressures on regulatory mechanisms of complex cognitive functions, including social cognition.

[1]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

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

[3]  J. Mcglone,et al.  Sex differences in human brain asymmetry: a critical survey , 1980, Behavioral and Brain Sciences.

[4]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[5]  B. Finlay,et al.  Developmental structure in brain evolution , 2001, Behavioral and Brain Sciences.

[6]  Nancy C Andreasen,et al.  Sexual dimorphism in the human brain: evaluation of tissue volume, tissue composition and surface anatomy using magnetic resonance imaging , 2000, Psychiatry Research: Neuroimaging.

[7]  Patrick R. Hof,et al.  Evolutionary Anatomy of the Primate Cerebral Cortex: Language areas of the hominoid brain: a dynamic communicative shift on the upper east side planum , 2001 .

[8]  J. Dejerine Anatomie des centres nerveux , 1895 .

[9]  Hanna Damasio,et al.  Sexual dimorphism and asymmetries in the gray–white composition of the human cerebrum , 2003, NeuroImage.

[10]  R. Lewin,et al.  Kanzi: The Ape at the Brink of the Human Mind , 1994 .

[11]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[12]  R. Holloway, Does allometry mask important brain structure residuals relevant to species-specific behavioral evolution? , 2001, Behavioral and Brain Sciences.

[13]  J. Allman,et al.  The Scaling of White Matter to Gray Matter in Cerebellum and Neocortex , 2003, Brain, Behavior and Evolution.

[14]  P. Benson,et al.  Recognizing one's own face , 2001, Cognition.

[15]  J. Goodall The Chimpanzees of Gombe: Patterns of Behavior , 1986 .

[16]  J. Jack,et al.  Electric current flow in excitable cells , 1975 .

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

[18]  A. Dagher,et al.  Mapping the network for planning: a correlational PET activation study with the Tower of London task. , 1999, Brain : a journal of neurology.

[19]  R. H. Biggerstaff The in vivo development of the hamster periodontium and implications for the chin's evolution. , 1973, American journal of physical anthropology.

[20]  Dennis Velakoulis,et al.  Individual differences in anterior cingulate/paracingulate morphology are related to executive functions in healthy males. , 2004, Cerebral cortex.

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

[22]  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.

[23]  J Tanji,et al.  Comparison of neuronal activity in the supplementary motor area and primary motor cortex. , 1996, Brain research. Cognitive brain research.

[24]  R. Holloway,,et al.  Brain endocast asymmetry in pongids and hominids: some preliminary findings on the paleontology of cerebral dominance. , 1982, American journal of physical anthropology.

[25]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[26]  R. Holloway, Chapter IV – Brain Size, Allometry, and Reorganization: Toward a Synthesis , 1979 .

[27]  H. Damasio,et al.  Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex , 1998, The Journal of Neuroscience.

[28]  B. Dudek,et al.  Development and evolution of brain size : behavioral implications , 1979 .

[29]  D Le Bihan,et al.  The Dorsolateral Prefrontal Cortex (dlpfc) Plays a Key Role in Working Memory (wm). yet Its Precise Contribution , 2022 .

[30]  R. J. Frank,et al.  Three-dimensional in vivo mapping of brain lesions in humans. , 1992, Archives of neurology.

[31]  A. Braun,et al.  Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. , 1998, Science.

[32]  D. Stuss,et al.  The frontal lobes are necessary for 'theory of mind'. , 2001, Brain : a journal of neurology.

[33]  S. Boysen Individual Differences in the Cognitive Abilities of Chimpanzees , 1994 .

[34]  S. Petersen,et al.  Hemispheric Specialization in Human Dorsal Frontal Cortex and Medial Temporal Lobe for Verbal and Nonverbal Memory Encoding , 1998, Neuron.

[35]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[36]  D. Stuss,et al.  Neuropsychological studies of the frontal lobes. , 1984, Psychological bulletin.

[37]  Alan C. Evans,et al.  Planning and Spatial Working Memory: a Positron Emission Tomography Study in Humans , 1996, The European journal of neuroscience.

[38]  R. Kötter,et al.  Functional dissociation between medial and lateral prefrontal cortical spatiotemporal activation in negative and positive emotions: a combined fMRI/MEG study. , 2000, Cerebral cortex.

[39]  Michael Tomasello,et al.  A Comparison of the Gestural Communication of Apes and Human Infants , 1997 .

[40]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[41]  A. Minkowski,et al.  Regional Development of the Brain in Early Life , 1968 .

[42]  M. Petrides Dissociable Roles of Mid-Dorsolateral Prefrontal and Anterior Inferotemporal Cortex in Visual Working Memory , 2000, The Journal of Neuroscience.

[43]  T. Sejnowski,et al.  A universal scaling law between gray matter and white matter of cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Graham Wideman,et al.  Gender differences in incidental learning and visual recognition memory : support for a sex difference in unconscious environmental awareness , 1998 .

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

[46]  M. Mishkin,et al.  Functional Mapping of the Primate Auditory System , 2003, Science.

[47]  T. L. Davis,et al.  Morphometry of in vivo human white matter association pathways with diffusion‐weighted magnetic resonance imaging , 1997, Annals of neurology.

[48]  H. J. Jerison,et al.  Evolution of the Brain and Intelligence , 1973 .

[49]  D. V. Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system , 1997, Nature.

[50]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[51]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[52]  Lennart Heimer The Human Brain and Spinal Cord , 1983 .

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

[54]  B. Turetsky,et al.  Sex Differences in Brain Gray and White Matter in Healthy Young Adults: Correlations with Cognitive Performance , 1999, The Journal of Neuroscience.

[55]  P. Hof,et al.  Is prefrontal white matter enlargement a human evolutionary specialization? , 2005, Nature Neuroscience.

[56]  R. Passingham The frontal cortex: does size matter? , 2002, Nature Neuroscience.

[57]  J. C. Redmond,et al.  Early hominid brain evolution: a new look at old endocasts. , 2000, Journal of human evolution.

[58]  C. V. van Schaik,et al.  The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): A tale of two islands , 2000 .

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

[60]  P. McGuire,et al.  Neural systems underlying British Sign Language and audio-visual English processing in native users. , 2002, Brain : a journal of neurology.

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

[62]  J. Rilling,et al.  Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys , 1998, Brain Research.

[63]  K. Gibson Evolution of Human Intelligence: The Roles of Brain Size and Mental Construction , 2002, Brain, Behavior and Evolution.

[64]  A. Schleicher,et al.  Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. , 1995, Journal of anatomy.

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

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

[67]  R. Knight,et al.  Frontal Lobe Contributions to Theory of Mind , 1998, Journal of Cognitive Neuroscience.

[68]  H. Damasio,et al.  Humans and great apes share a large frontal cortex , 2002, Nature Neuroscience.

[69]  J. Cummings Frontal-subcortical circuits and human behavior. , 1993, Journal of psychosomatic research.

[70]  Eric Courchesne,et al.  Localized enlargement of the frontal cortex in early autism , 2005, Biological Psychiatry.

[71]  D. Tautz,et al.  Mitochondrial sequences show diverse evolutionary histories of African hominoids. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[73]  Albert M. Galaburda,et al.  Cerebral dominance : the biological foundations , 1984 .

[74]  J. Sundsten,et al.  Folding of the Cerebral Cortex in Mammals , 1984 .

[75]  Anne E. Russon,et al.  Return of the Native: Cognition and Site-Specific Expertise in Orangutan Rehabilitation , 2002, International Journal of Primatology.

[76]  A. Damasio,et al.  A role for left temporal pole in the retrieval of words for unique entities , 2001, Human brain mapping.

[77]  A. Schleicher,et al.  Gyrification in the cerebral cortex of primates. , 1989, Brain, behavior and evolution.

[78]  Richard D. Hichwa,et al.  A neural basis for lexical retrieval , 1996, Nature.

[79]  P. Schoenemann,et al.  Prefrontal white matter volume is disproportionately larger in humans than in other primates , 2005, Nature Neuroscience.

[80]  Michael Vannier,et al.  Human cortical asymmetries determined with 3D MR technology , 1991, Journal of Neuroscience Methods.

[81]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[82]  J. Ehrhardt,et al.  Regional brain abnormalities in schizophrenia measured with magnetic resonance imaging. , 1994, JAMA.

[83]  N. Makris,et al.  MRI-Based Topographic Parcellation of Human Neocortex: An Anatomically Specified Method with Estimate of Reliability , 1996, Journal of Cognitive Neuroscience.

[84]  David A. Ziegler,et al.  Localization of white matter volume increase in autism and developmental language disorder , 2004, Annals of neurology.

[85]  S. Petersen,et al.  Wada Testing Reveals Frontal Lateralization for the Memorization of Words and Faces , 2002, Journal of Cognitive Neuroscience.

[86]  R. Passingham The Human Primate , 1982 .

[87]  Rex E. Jung,et al.  The neuroanatomy of general intelligence: sex matters , 2005, NeuroImage.

[88]  C. Price,et al.  Identification of famous faces and buildings: a functional neuroimaging study of semantically unique items. , 2001, Brain : a journal of neurology.

[89]  Eileen Luders,et al.  Gender differences in cortical complexity , 2004, Nature Neuroscience.

[90]  N C Andreasen,et al.  The neuropsychology of the prefrontal cortex. , 1993, Archives of neurology.

[91]  A. Schleicher,et al.  The human pattern of gyrification in the cerebral cortex , 2004, Anatomy and Embryology.

[92]  A. Foundas The Anatomical Basis of Language. , 2001 .

[93]  Joseph Glicksohn,et al.  The representation of patterns of structural brain asymmetry in normal individuals , 1993, Neuropsychologia.

[94]  Eric Courchesne,et al.  Cerebral Lobes in Autism: Early Hyperplasia and Abnormal Age Effects , 2002, NeuroImage.

[95]  Eric E. Nelson,et al.  Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants , 2004, NeuroImage.

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

[97]  S. Wang,et al.  Scaling laws in the mammalian neocortex: Does form provide clues to function? , 2002, Journal of neurocytology.

[98]  K. Semendeferi Evolutionary Anatomy of the Primate Cerebral Cortex: Advances in the study of hominoid brain evolution: magnetic resonance imaging (MRI) and 3-D reconstruction , 2001 .

[99]  John S. Allen,et al.  Normal neuroanatomical variation in the human brain: an MRI-volumetric study. , 2002, American journal of physical anthropology.

[100]  Lina Shihabuddin,et al.  MRI assessment of gray and white matter distribution in Brodmann's areas of the cortex in patients with schizophrenia with good and poor outcomes. , 2003, The American journal of psychiatry.

[101]  P. Harvey,et al.  Mosaic evolution of brain structure in mammals , 2000, Nature.

[102]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[103]  G. Schoenbaum,et al.  Integrating orbitofrontal cortex into prefrontal theory: common processing themes across species and subdivisions. , 2001, Learning & memory.

[104]  G. V. Van Hoesen,et al.  The evolution of the frontal lobes: a volumetric analysis based on three-dimensional reconstructions of magnetic resonance scans of human and ape brains. , 1997, Journal of human evolution.

[105]  W. Hopkins,et al.  Asymmetries in cerebral width in nonhuman primate brains as revealed by magnetic resonance imaging (MRI) , 2000, Neuropsychologia.

[106]  W D Hopkins,et al.  A comparative MRI study of the relationship between neuroanatomical asymmetry and interhemispheric connectivity in primates: implication for the evolution of functional asymmetries. , 2000, Behavioral neuroscience.