Variability and asymmetry of the sulcal contours defining Broca's area homologue in the chimpanzee brain

There has been recent motivation to search for neuroanatomical asymmetries in nonhuman primates in order to provide comparative information on how the human brain is structurally organized to support specific cognitive capabilities, such as language functions. We took the opportunity to study Broca's area homologue in a novel sample of 80 preserved postmortem chimpanzee (Pan troglodytes) cerebral hemispheres. Consistent with the only prior study documenting the morphology of Broca's area homologue in the chimpanzee (Sherwood et al. [2003] Anat Rec 271:276–285), we report great interindividual variation in the structure and connections of the sulci investigated, most notably a left‐sided bias in the bifurcation of the inferior precentral sulcus, an anatomical feature that occurs much more frequently in chimpanzees relative to humans. Consistent with our recent neuroimaging report (Keller et al. [2009b] J Neurosci 29:14607–14616), no population‐based interhemispheric asymmetries of sulcal length existed that could be considered markers of the size of Broca's area homologue. With strict anatomical guidelines, we report that the diagonal sulcus was present in 25% left and 20% right chimpanzee hemispheres studied, which is substantially less that the general prevalence in humans. Through the presentation of schematic drawings, photographs, morphological recordings and sulcal length metrics, our data illustrate the interindividual variability of Broca's area homologue in the chimpanzee and support the notion of no macroscopic asymmetry of this important homologous language brain region in one of the closest evolutionary ancestor to modern humans J. Comp. Neurol. 520:1165–1180, 2012. © 2011 Wiley Periodicals, Inc.

[1]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[2]  Jamie L. Russell,et al.  Communicative Signaling Activates ‘Broca's’ Homolog in Chimpanzees , 2008, Current Biology.

[3]  E. Ringelstein,et al.  Handedness and hemispheric language dominance in healthy humans. , 2000, Brain : a journal of neurology.

[4]  D. J. Cunningham,et al.  Contribution to the surface anatomy of the cerebral hemispheres . with A chapter upon cranio-cerebral topography , 1892 .

[5]  Katrin Amunts,et al.  Broca’s area: Nomenclature, anatomy, typology and asymmetry , 2009, Brain and Language.

[6]  E. Ringelstein,et al.  Language lateralization in healthy right-handers. , 2000, Brain : a journal of neurology.

[7]  William D. Hopkins,et al.  Gray matter asymmetries in chimpanzees as revealed by voxel-based morphometry , 2008, NeuroImage.

[8]  K M Heilman,et al.  Anomalous anatomy of speech–language areas in adults with persistent developmental stuttering , 2001, Neurology.

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

[10]  A Merlo,et al.  Anterior speech region. Asymmetry and weight-surface correlation. , 1989, Archives of neurology.

[11]  M. García-Fiñana,et al.  Sulcal variability, stereological measurement and asymmetry of Broca's area on MR images , 2007, Journal of anatomy.

[12]  William D Hopkins,et al.  Gesture handedness predicts asymmetry in the chimpanzee inferior frontal gyrus , 2006, Neuroreport.

[13]  G A Ojemann,et al.  Individual variability in cortical localization of language. , 1979, Journal of neurosurgery.

[14]  Michael Petrides,et al.  Precentral sulcal complex of the human brain: Morphology and statistical probability maps , 2005, The Journal of comparative neurology.

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

[16]  T. Nir,et al.  The chimpanzee brain shows human‐like perisylvian asymmetries in white matter , 2009, The European journal of neuroscience.

[17]  William D Hopkins,et al.  Neuroanatomical Correlates of Handedness for Tool Use in Chimpanzees (Pan Troglodytes) , 2007, Psychological science.

[18]  Stefan Knecht,et al.  Can the Language-dominant Hemisphere Be Predicted by Brain Anatomy? , 2011, Journal of Cognitive Neuroscience.

[19]  S. F. Witelson,et al.  Intelligence and brain size in 100 postmortem brains: sex, lateralization and age factors. , 2006, Brain : a journal of neurology.

[20]  Giorgio M. Innocenti,et al.  PATHWAYS BETWEEN DEVELOPMENT AND EVOLUTION , 1991 .

[21]  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 .

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

[23]  Q. Mcnemar Note on the sampling error of the difference between correlated proportions or percentages , 1947, Psychometrika.

[24]  David L. Cooper,et al.  Broca's arrow: evolution, prediction, and language in the brain. , 2006, Anatomical record. Part B, New anatomist.

[25]  Neil Roberts,et al.  A Comparative Magnetic Resonance Imaging Study of the Anatomy, Variability, and Asymmetry of Broca's Area in the Human and Chimpanzee Brain , 2009, The Journal of Neuroscience.

[26]  Patrick R Hof,et al.  Broca's area homologue in chimpanzees (Pan troglodytes): probabilistic mapping, asymmetry, and comparison to humans. , 2009, Cerebral cortex.

[27]  William D Hopkins,et al.  Handedness is associated with asymmetries in gyrification of the cerebral cortex of chimpanzees. , 2007, Cerebral cortex.

[28]  K. Amunts,et al.  A multimodal analysis of the structure and function in Broca's region , 2006 .

[29]  A M Galaburda,et al.  The human language areas and cerebral asymmetries. , 1980, Revue medicale de la Suisse romande.

[30]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[31]  H. Goddard Intelligence and will. , 1919 .

[32]  Anne L. Foundas,et al.  Anatomical Asymmetries of Anterior Perisylvian Speech-Language Regions , 2007, Cortex.

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

[34]  Katrin Amunts,et al.  The central sulcus: an observer-independent characterization of sulcal landmarks and depth asymmetry. , 2008, Cerebral cortex.

[35]  Henry Kennedy,et al.  Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: Effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex , 1996, The Journal of comparative neurology.

[36]  J. Kaas,et al.  Connectivity-driven white matter scaling and folding in primate cerebral cortex , 2010, Proceedings of the National Academy of Sciences.

[37]  G. Flandin,et al.  Predicting Language Lateralization from Gray Matter , 2009, The Journal of Neuroscience.

[38]  T. L. Hayes,et al.  Anatomical Specialization of the Anterior Motor Speech Area: Hemispheric Differences in Magnopyramidal Neurons , 1995, Brain and Language.

[39]  William D Hopkins,et al.  Handedness in chimpanzees (Pan troglodytes) is associated with asymmetries of the primary motor cortex but not with homologous language areas. , 2004, Behavioral neuroscience.

[40]  Robert J Zatorre,et al.  Asymmetries of the planum temporale and Heschl's gyrus: relationship to language lateralization. , 2006, Brain : a journal of neurology.

[41]  K M Heilman,et al.  Pars triangularis asymmetry and language dominance. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[44]  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.

[45]  William D Hopkins,et al.  The Association between handedness, brain asymmetries, and corpus callosum size in chimpanzees (Pan troglodytes). , 2007, Cerebral cortex.

[46]  P. Perrone,et al.  Right-left asymmetry in anterior speech region. , 1982, Archives of neurology.

[47]  R. Quester,et al.  The shrinkage of the human brain stem during formalin fixation and embedding in paraffin , 1997, Journal of Neuroscience Methods.

[48]  P. García-López,et al.  Sculpting the brain , 2012, Front. Hum. Neurosci..

[49]  Vitaly A Klyachko,et al.  Connectivity optimization and the positioning of cortical areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[51]  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.

[52]  T. L. Hayes,et al.  Hemispheric differences in layer III pyramidal neurons of the anterior language area. , 1993, Archives of neurology.

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

[54]  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.