Gray matter asymmetries in chimpanzees as revealed by voxel-based morphometry

Determination of whether nonhuman primates exhibit neuroanatomical asymmetries would inform our understanding of the evolution of traits in humans that show functional hemispheric dominance, including language and handedness. Here we report the first evidence of population-level asymmetries in the chimpanzee neocortex using voxel-based morphometry (VBM). MRI scans of the brain were collected in a sample of 31 chimpanzees including 9 males and 22 females, and the resulting images were segmented into gray matter, white matter and CSF. Gray matter images were then co-registered to a template and these normally oriented volumes were flipped on the left-right axis to create mirror volumes. In total, significant asymmetries were found in 13 regions including several that have been described previously in great apes using traditional region-of-interest approaches. The results from this VBM analysis support previous reports of hemispheric lateralization in chimpanzees and reinforce the view that asymmetries in the central nervous system are not uniquely human.

[1]  G. Ettlinger.  Hand Preference, Ability, Hemispheric Specialization: In How Far are these Factors Related in the Monkey? , 1988, Cortex.

[2]  J. Rilling,et al.  Planum temporale asymmetries in great apes as revealed by magnetic resonance imaging (MRI) , 1998, Neuroreport.

[3]  Lutz Jäncke,et al.  A voxel-based approach to gray matter asymmetries , 2004, NeuroImage.

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

[5]  L. Rogers.  Comparative Vertebrate Lateralization: Preface , 2002 .

[6]  Alan P. Neuren.  The Lopsided Ape , 1992, Neurology.

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

[8]  William D Hopkins,et al.  Are planum temporale and sylvian fissure asymmetries directly related? A MRI study in great apes , 2003, Neuropsychologia.

[9]  T. Crow,et al.  Accelerated evolution of Protocadherin11X/Y: A candidate gene‐pair for cerebral asymmetry and language , 2006, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[10]  Timothy J. Crow,et al.  Directional asymmetry is the key to the origin of modern Homo sapiens (the Broca‐Annett axiom): A reply to Rogers' review of The Speciation of Modern Homo Sapiens , 2004 .

[11]  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.

[12]  William D. Hopkins,et al.  Sylvian Fissure Asymmetries in Nonhuman Primates Revisited: A Comparative MRI Study , 2000, Brain, Behavior and Evolution.

[13]  Karl J. Friston,et al.  Cerebral Asymmetry and the Effects of Sex and Handedness on Brain Structure: A Voxel-Based Morphometric Analysis of 465 Normal Adult Human Brains , 2001, NeuroImage.

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

[15]  A. David,et al.  The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance , 1999, Brain Research Reviews.

[16]  D. Weinberger,et al.  MRI Asymmetries of Broca's Area: The Pars Triangularis and Pars Opercularis , 1998, Brain and Language.

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

[18]  Dirk Vandermeulen,et al.  Automatic analysis of cerebral asymmetry: an exploratory study of the relationship between brain torque and planum temporale asymmetry , 2005, NeuroImage.

[19]  A. Beaton,et al.  The Relation of Planum Temporale Asymmetry and Morphology of the Corpus Callosum to Handedness, Gender, and Dyslexia: A Review of the Evidence , 1997, Brain and Language.

[20]  N. Geschwind,et al.  Asymmetries of the Brains and Skulls of Nonhuman Primates , 1982 .

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

[22]  A. Damasio,et al.  The neural basis of language. , 1984, Annual review of neuroscience.

[23]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[24]  J. M. Warren,et al.  Handedness and laterality in humans and other animals , 1980 .

[25]  W. Hopkins.  The evolution of hemispheric specialization in primates , 2007 .

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

[27]  W. Hopkins,et al.  Cerebral volumetric asymmetries in non-human primates: A magnetic resonance imaging study , 2001, Laterality.

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