Research report
Planum temporale surface area and grey matter asymmetries in chimpanzees (Pan troglodytes): The effect of handedness and comparison with findings in humans

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Abstract

The planum temporale (PT) is the bank of tissue that lies posterior to Heschl's gyrus and is considered a key brain region involved in language and speech in the human brain. In the human brain, both the surface area and grey matter volume of the PT is larger in the left compared to right hemisphere in approximately 2/3rds of individuals, particularly among right-handed individuals. Here we examined whether chimpanzees show asymmetries in the PT for grey matter volume and surface area in a sample of 103 chimpanzees from magnetic resonance images. The results indicated that, overall, the chimpanzees showed population-level leftward asymmetries for both surface area and grey matter volumes. Furthermore, chimpanzees that prefer to gesture with their right-handed had significantly greater leftward grey matter asymmetries compared to ambiguously- and left-handed apes. When compared to previously published data in humans, the direction and magnitude of PT grey matter asymmetries were similar between humans and apes; however, for the surface area measures, the human showed more pronounced leftward asymmetries. These results suggest that leftward asymmetries in the PT were present in the common ancestor of chimpanzees and humans.

Section snippets

Subjects

Magnetic resonance images were obtained from a sample of 103 chimpanzees including 41 males and 62 females. The subjects ranged in age from 6 to 51 years (mean = 24.736, s.d. = 11.91). All the chimpanzees were members of a captive colony housed at Yerkes National Primate Research Center (YNPRC) in Atlanta, Georgia. All procedures used with the chimpanzees were approved by the Institutional Animal Care and Use Committee of Emory University. Shown in Table 1 are the handedness distributions and the

Descriptive statistics

The left and right PT surface areas and grey matter volumes for each scanner type are shown in Table 2. In the initial analyses, we compared the left and right PT areas and GM volumes between sexes (male, female) and the scanner type (1.5, 3.0 and cadaver) using a mixed model ANOVA. Hemisphere was the repeated measure while sex and scanner types were the between group factors. For the PT surface area, a significant main effect for hemisphere was found F(1, 99) = 28.36, p < .001 with the left PT

Discussion

Two main results emerged from this study. First, chimpanzees show significant population-level leftward asymmetries in the planum temporale when measuring both the surface area and the grey matter volumes. Second, chimpanzees that prefer to gesture with the right hand show significantly greater leftward asymmetries in the grey matter volume of the PT compared to left-handed individuals. Hand preferences for non-communicative functions were not associated with asymmetries in either the surface

Acknowledgments

This research was supported in part by NIH grants NS-36605, NS-42867, HD-38051, and HD-56232. The Yerkes Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care. American Psychological Association guidelines for the ethical treatment of animals were adhered to during all aspects of this study. We are grateful to the helpful assistance of the entire veterinary staff at the Yerkes Center for their assistance in collection of the MRI scans.

References (79)

  • D. Falk et al.

    Cortical asymmetries in the frontal lobe of rhesus monkeys (Macaca mulatta)

    Brain Research

    (1990)
  • C. Cantalupo et al.

    Are planum temporale and sylvian fissure asymmetries directly related? a MRI study in great apes

    Neuropsychologia

    (2003)
  • T. Zetzsche et al.

    In-vivo analysis of human planum temporale (PT): does the definition of PT borders influence the resulys with regard to cerebral asymmetry and correlation with handedness?

    Psychiatry Research: Neuroimaging Section

    (2001)
  • T.A. Knaus et al.

    Variability in perisylvian brain anatomy in healthy adults

    Brain and Language

    (2006)
  • M. Annett

    Handedness and brain asymmetry: the right shift theory

    (2002)
  • J.L. Bradshaw et al.

    The evolution of lateral asymmetries, language, tool use, and intellect

    (1993)
  • M.C. Corballis

    The lopsided brain: evolution of the generative mind

    (1992)
  • M.C. Corballis

    From hand to mouth: the origins of language

    (2002)
  • R.J. Davidson

    Cerebral asymmetry, emotion and affective style

  • A.W. Toga et al.

    Mapping brain asymmetry

    Nature

    (2003)
  • A.M. Galaburda

    Anatomic basis of cerebral dominance

  • N. Geschwind et al.

    Human brain: left-right asymmetries in temporal speech region

    Science

    (1968)
  • K.E. Watkins et al.

    Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans

    Cerebral Cortex

    (2001)
  • J. Pekkola et al.

    Attention to visual speech gestures enhances hemodynamic activity in the left planum temporale

    Human Brain Mapping

    (2006)
  • R. Raquel Dorsaint-Pierre et al.

    Asymmetries of the planum temporale and Heschl's gyrus: relationship to language lateralization

    Brain

    (2006)
  • J.M. Rumsey et al.

    A magnetic resonance imaging study of planum temporale asymmetry in men with developmental dyslexia

    Archives of Neurology

    (1997)
  • I. Sommer et al.

    Handedness, language lateralisation and anatomical asymmetry in schizophrenia: Meta-analysis

    British Journal of Psychiatry

    (2001)
  • I.E.C. Sommer et al.

    Do women really have more bilateral language representation than men? A meta-analysis of functional imaging studies

    Brain

    (2004)
  • S.F. Witelson et al.

    Sylvian fissure morphology and asymmetry in men and women: bilateral differences in relation to handedness in men

    Journal of Comparative Neurology

    (1992)
  • T. Hatta

    Handedness and the brain: a review of brain-imaging techniques

    Magnetic Resonance in Medical Science

    (2006)
  • J.J. Kulynych et al.

    Gender differences in the normal lateralization of the supratemporal cortex: MRI surface-rendering morphometry of Heschl's gyrus and the planum temporale

    Cerebral Cortex

    (1994)
  • T.A. Knaus et al.

    Sex-linked differences in the anatomy of the persi-sylvian language cortex: a volumetric MRI study of gray matter volumes

    Neuropsychology

    (2004)
  • A. Foundas et al.

    Morphological cerebral asymmetries and handedness: the pars triangularis and planum temporale

    Archives of Neurology

    (1995)
  • H. Steinmetz et al.

    Anatomical left-right asymmetry of language-related temporal cortex is different in left- and right-handers

    Annals of Neurology

    (1991)
  • G. Yeni-Komshian et al.

    Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees and monkeys

    Science

    (1976)
  • D. Falka et al.

    Advanced computer-graphics technology reveals cortical asymmetry in endocasts of rhesus-monkeys

    Folia Primatologica

    (1986)
  • P.L. Heilbronner et al.

    Anatomical brain asymmetries in New World and Old World monkeys. Stages of temporal lobe development in primate evolution

    American Journal of Physical Anthropology

    (1988)
  • E. Gilissen

    The neocortical sulci of the capuchin monkey (Cebus): evidence for asymmetry in the sylvian sulcus and comparison with other primates

    Comptes Rendus de l’Academie de Sciences Paris, Series III

    (1992)
  • P.J. Gannon et al.

    Asymmetry of chimpanzee Planum Temporale: Humanlike pattern of Wernicke's language area homolog

    Science

    (1998)
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