Handedness is associated with asymmetries in gyrification of the cerebral cortex of chimpanzees.

Gyrification of the cerebral cortex reflects complexity in cortical folding during development of the brain. In this paper, we evaluated whether chimpanzees show asymmetries in gyrification and if variation in gyrification asymmetries were associated with handedness. Magnetic resonance images were obtained in a sample of 76 chimpanzees, and gyrification measures were obtained from 10 equally spaced slices of the cortex. Asymmetry quotients (AQs) in gyrification were compared for 4 measures of handedness including reaching, coordinated bimanual actions, manual gestures, and throwing. Overall, the chimpanzees showed significant differences between the right and left hemispheres that were region specific. Significant differences in AQ's were found in right- and nonright-handed chimpanzees for throwing and, to a lesser degree, for manual gestures. Increasing age was associated with increasing gyrification in the prefrontal regions, particularly in female chimpanzees. The results indicate that variation in gyrification between hemispheres is associated with functional measures of laterality in chimpanzees.

[1]  Karl Zilles,et al.  Cortical folding and the evolution of the human brain , 1993 .

[2]  William D Hopkins,et al.  The Distribution and Development of Handedness for Manual Gestures in Captive Chimpanzees (Pan troglodytes) , 2005, Psychological science.

[3]  A. Hostetter,et al.  Grip morphology and hand use in chimpanzees (Pan troglodytes): evidence of a left hemisphere specialization in motor skill. , 2002, Journal of experimental psychology. General.

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

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

[6]  A. Schleicher,et al.  Quantitative analysis of gyrification of cerebral cortex in dogs. , 1996, Neurobiology.

[7]  S. Schapiro,et al.  Chimpanzees (Pan troglodytes) are predominantly right-handed: replication in three populations of apes. , 2004, Behavioral neuroscience.

[8]  J. Mazziotta,et al.  Age‐related morphology trends of cortical sulci , 2005, Human brain mapping.

[9]  J. Rilling Human and nonhuman primate brains: Are they allometrically scaled versions of the same design? , 2006 .

[10]  W. McGrew,et al.  On the Other Hand: Current Issues in and Meta-Analysis of the Behavioral Laterality of Hand Function in Nonhuman Primates , 1997 .

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

[12]  Eve C Johnstone,et al.  Abnormal cortical folding in high-risk individuals: a predictor of the development of schizophrenia? , 2004, Biological Psychiatry.

[13]  M. Gazzaniga,et al.  The new cognitive neurosciences , 2000 .

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

[15]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

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

[17]  Jamie L. Russell,et al.  Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). , 2005, Journal of comparative psychology.

[18]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.

[19]  Julio M. Araque,et al.  Reduced Brain Size and Gyrification in the Brains of Dyslexic Patients , 2004, Journal of child neurology.

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

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

[22]  D. Washburn Primate Perspectives on Behavior and Cognition , 2006 .

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

[24]  T. Cizadlo,et al.  Quantitative in vivo measurement of gyrification in the human brain: changes associated with aging. , 1999, Cerebral cortex.

[25]  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.

[26]  T. Insel,et al.  Differential expansion of neural projection systems in primate brain evolution. , 1999, Neuroreport.

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

[28]  J. Tigges,et al.  Brain weight throughout the life span of the chimpanzee , 1999, The Journal of comparative neurology.

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

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

[31]  S. Williams-Blangero,et al.  Future Costs of Chimpanzees in U.S. Research Institutions. , 1995, ILAR journal.

[32]  A. Schleicher,et al.  The ontogeny of human gyrification. , 1995, Cerebral cortex.

[33]  W. Hopkins,et al.  Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis. , 1995, Journal of comparative psychology.

[34]  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.

[35]  Marjorie LeMay,et al.  MORPHOLOGICAL CEREBRAL ASYMMETRIES OF MODERN MAN, FOSSIL MAN, AND NONHUMAN PRIMATE , 1976, Annals of the New York Academy of Sciences.

[36]  N. Andreasen,et al.  Gyrification abnormalities in childhood- and adolescent-onset schizophrenia , 2003, Biological Psychiatry.

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

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

[39]  T. Insel,et al.  Evolution of the Cerebellum in Primates: Differences in Relative Volume among Monkeys, Apes and Humans , 1998, Brain, Behavior and Evolution.

[40]  T M Mayhew,et al.  The gyrification of mammalian cerebral cortex: quantitative evidence of anisomorphic surface expansion during phylogenetic and ontogenetic development. , 1996, Journal of anatomy.

[41]  K Zilles,et al.  Cortical gyrification in the rhesus monkey: a test of the mechanical folding hypothesis. , 1991, Cerebral cortex.

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

[43]  Karl Zilles,et al.  Cortical folding, the lunate sulcus and the evolution of the human brain , 1991 .

[44]  D. Weinberger,et al.  Asymmetrical volumes of the right and left frontal and occipital regions of the human brain , 1982, Annals of neurology.