A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca's area in humans and great apes

Broca's area was identified in the inferior frontal gyrus of chimpanzee, bonobo, gorilla, and orangutan brains through direct cytoarchitectonic comparison with human brains. Across species, Broca's area comprises Brodmann's areas 44 and 45. We found that these areas exhibited similar cytoarchitectonic characteristics in all species examined. We analyzed the minicolumnar organization of cells in layer III of Broca's area in 11 human and 9 great ape specimens. A semiautomated method was used to analyze digitized images of histological sections stained for Nissl substance. Horizontal spacing distance and gray level index (GLI; or the area fraction occupied by cells) were quantified in all images. In contrast to area Tpt, the only cortical area for which comparative minicolumnar data have been published previously for humans and one of the great apes, we found no population‐level asymmetry, for either horizontal spacing distance or GLI. Only human females exhibited a leftward asymmetry in GLI. GLI was lower in humans than in great apes (P < 0.001), allowing more space for connectivity in layer III. In humans, horizontal spacing distance was greater than in great apes but smaller relative to brain size. J. Comp. Neurol. 510:117–128, 2008. © 2008 Wiley‐Liss, Inc.

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

[2]  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.

[3]  S. Pääbo,et al.  Intra- and Interspecific Variation in Primate Gene Expression Patterns , 2002, Science.

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

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

[6]  J. Lübke,et al.  Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex , 2007, Brain Structure and Function.

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

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

[9]  H. Barbas,et al.  Cortical structure predicts the pattern of corticocortical connections. , 1997, Cerebral cortex.

[10]  S. Wacquant,et al.  A columnar model of somatosensory reorganizational plasticity based on Hebbian and non-Hebbian learning rules , 1996, Biological Cybernetics.

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

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

[13]  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.

[14]  Joel L. Davis,et al.  Single neuron computation , 1992 .

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

[16]  A. Anwander,et al.  Connectivity-Based Parcellation of Broca's Area. , 2006, Cerebral cortex.

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

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

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

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

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

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

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

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

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

[26]  Patrick R. Hof,et al.  Leftward interhemispheric asymmetry of macaque monkey temporal lobe language area homolog is evident at the cytoarchitectural, but not gross anatomic level , 2008, Brain Research.

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

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

[29]  T. J. Crow,et al.  Minicolumnar structure in Heschl’s gyrus and planum temporale: Asymmetries in relation to sex and callosal fiber number , 2006, Neuroscience.

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

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

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

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

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

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

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

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

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

[39]  Thomas C. Hales,et al.  The Honeycomb Conjecture , 1999, Discret. Comput. Geom..

[40]  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.

[41]  Nathalie Tzourio-Mazoyer,et al.  Hemispheric specialization for language , 2004, Brain Research Reviews.

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

[43]  V. Mountcastle.  The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

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

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

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

[47]  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.

[48]  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.

[49]  U. Yinon,et al.  Columnar organization of the mammalian visual cortex and its vulnerability following lesion in adult cats , 2005, Brain injury.

[50]  P. Hof,et al.  Microstructural Asymmetries of the Cerebral Cortex in Humans and Other Mammals , 2007 .

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

[52]  Claus C. Hilgetag,et al.  Rules relating connections to cortical structure in primate prefrontal cortex , 2002, Neurocomputing.

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

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

[55]  M. Diamond,et al.  Demonstration of discrete place‐defined columns—segregates—in the cat SI , 1990, The Journal of comparative neurology.

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

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

[58]  G. Bruyn.  Atlas of the Cerebral Sulci, M. Ono, S. Kubik, Chad D. Abernathey (Eds.). Georg Thieme Verlag, Stuttgart, New York (1990), 232, DM 298 , 1990 .

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

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

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

[62]  B L Whitsel,et al.  Minicolumnar activation patterns in cat and monkey SI cortex. , 1993, Cerebral cortex.

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

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

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

[66]  Giuseppe Pagnoni,et al.  A comparison of resting-state brain activity in humans and chimpanzees , 2007, Proceedings of the National Academy of Sciences.

[67]  Donald Favareau.  The Symbolic Species: The Co-evolution of Language and the Brain , 1998 .

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

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

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

[71]  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.

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

[73]  C. Büchel,et al.  Broca's area and the language instinct , 2003, Nature Neuroscience.

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

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

[76]  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.

[77]  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.

[78]  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.

[79]  G. Shepherd,et al.  Geometric and functional organization of cortical circuits , 2005, Nature Neuroscience.

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

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

[82]  A. Schleicher,et al.  Quantitative analysis of the columnar arrangement of neurons in the human cingulate cortex , 1995, The Journal of comparative neurology.