Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-17T23:26:53.567Z Has data issue: false hasContentIssue false
  • English
  • Français

On the biological basis of human laterality: II. The mechanisms of inheritance

Published online by Cambridge University Press:  04 February 2010

Michael J. Morgan  and
Michael C. Corballis
Michael J. Morgan
Affiliation:
Department of Psychology, University of Durham, Durham OH1 3LE, England
Michael C. Corballis
Affiliation:
Department of Psychology, University of Auckland, Auckland, New Zealand
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper focuses on the inheritance of human handedness and cerebral lateralization within the more general context of structural biological asymmetries. The morphogenesis of asymmetrical structures, such as the heart in vertebrates, depends upon a complex interaction between information coded in the cytoplasm and in the genes, but the polarity of asymmetry seems to depend on the cytoplasmic rather than the genetic code. Indeed it is extremely difficult to find clear-cut examples in which the direction of an asymmetry is under genetic control. As one possible case, there is some evidence that the direction, clockwise or counterclockwise, of rotation of the abdomen in certain mutant strains of Drosophila is controlled by a particular gene locus, although there appears to be some degree of confusion on this point. By contrast, it is much easier to find examples in which the degree but not the direction of asymmetry is under genetic control. For instance, there is a mutant strain of mice in which half of the animals display situs inversus of the viscera. The proportion has remained at one half despite many years of inbreeding, suggesting that the mutant allele effectively cancels the normal situs and allows the asymmetry to be specified in random fashion.

Although this account does not deny that the right hemisphere of humans may be the more specialized for certain functions, it does attribute a leading or dominant role to the left hemisphere (at least in most individuals). We suggest that so-called “right-hemisphere” functions are essentially acquired by default, due to the left hemisphere's prior involvement with speech and skilled motor acts; we note, for instance, that these right-hemisphere functions include rather elementary perceptual processes. But perhaps the more critical prediction from our account is that the phenomenon of equipotentiality should be unidirectional: the right (lagging) hemisphere should be more disposed to take over left-hemisphere functions following early lesions than is the left (leading) hemisphere to take over right-hemisphere functions. We note preliminary evidence that this may be so.

Keywords

asymmetrycerebral dominancegeneticshandednesslaterality
Type
Target Article
Information
Behavioral and Brain Sciences , Volume 1 , Issue 2 , June 1978 , pp. 270 - 277
Copyright
Copyright © Cambridge University Press 1978

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Annett, M.The distribution of manual asymmetry. British Journal of Psychology. 63:343–58. 1972.CrossRefGoogle ScholarPubMed
Annett, M.Handedness in the children of two left-handed parents. British Journal of Psychology. 65:129–31. 1974.CrossRefGoogle ScholarPubMed
Bakan, P.Birth order and handedness. Nature. 229:195. 1971.CrossRefGoogle ScholarPubMed
Bakan, P., Dibb, G., & Reed, P.Handedness and birth stress. Neuropsychologia. 11:363–66. 1973.CrossRefGoogle ScholarPubMed
Bradley, B. P.Asymmetry of development under stabilizing selection in constant and fluctuating environments. Genetics. 77:55–56 (abstract). 1974.Google Scholar
Breitenbrecher, J. K.The inheritance of sex-limited bilateral asymmetry in Bruchus. Genetics. 10:261–77. 1925.CrossRefGoogle Scholar
Bridges, C. B., & Brehme, K. S.The mutants of Drosophila melanogaster. Washington, D.C.: The Carnegie Institute, Publication No. 552. 1944.Google Scholar
Brinkman, J. & Kuypers, H. G. J. M.Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. Brain. 96:653–74. 1973.CrossRefGoogle ScholarPubMed
Bryden, M. P.Speech lateralization in families: A preliminary study using dichotic listening. Brain & Language. 2:201–11. 1975.CrossRefGoogle ScholarPubMed
Chamberlain, H. D.The inheritance of left handedness. Journal of Heredity. 19:557–59. 1928.CrossRefGoogle Scholar
Collins, R. L.On the inheritance of handedness: II. Selection for sinistrality in mice. Journal of Heredity. 60:117–19. 1969.CrossRefGoogle ScholarPubMed
Collins, R. L. The sound of one paw clapping: An inquiry into the origin of left-handedness. In: Lindzey, G. & Thiessen, D. D. (eds.), Contributions to behavior-genetic analysis - The mouse as a prototype. New York: Meredith Corporation, 1970.Google Scholar
Collins, R. L.When left-handed mice live in right-handed worlds. Science. 187:181–84. 1975.CrossRefGoogle ScholarPubMed
Collins, R. L. Towards a permissible genetic model for the inheritance of the degree and direction of asymmetry. In: Harnad, S. R., Doty, R. W., Goldstein, L., Jaynes, J., & Krauthamer, G. (eds.), Lateralization in the nervous system. New York: Academic Press, 1977.Google Scholar
Corballis, M. C. Is left handedness genetically determined? In: Herron, J. (ed.), The sinistral mind. New York: Academic Press (in press).Google Scholar
Corballis, M. C. & Beale, I. L.The psychology of left and right. Hillsdale, N.J.: Lawrence Erlbaum Associates, 1976.Google Scholar
Dahlberg, G.Genotypic asymmetries. Proceedings of the Royal Society of Edinburgh. 63:20–31. 1943.Google Scholar
Davidson, E. H.Gene activity in early development. New York: Academic Press, 1968.Google Scholar
Fogh-Andersen, P.Inheritance of harelip and cleft palate. Opera ex Domo biologiae hereditariae humanae Universitatis hafniensis. 4:266 pp. 1943. (cited by Stern, 1955).Google Scholar
Gardner, M.The ambidextrous universe. London: Allen Lane, The Penguin Press, 1964.Google Scholar
Gesell, A., & Ames, L. B.The development of handedness. Journal of Genetic Psychology. 70:155–75. 1947.Google ScholarPubMed
Goodglass, H., & Quadfasel, F. A.Language laterality in left-handed aphasics. Brain. 77:521–48. 1954.CrossRefGoogle ScholarPubMed
Hécaen, H., & Sauguet, J.Cerebral dominance in left-handed subjects. Cortex. 7:19–48. 1971.CrossRefGoogle ScholarPubMed
Hicks, R. E., & Kinsbourne, M.Human handedness: A partial cross-fostering study. Science. 192:908–10. 1976.CrossRefGoogle ScholarPubMed
Hines, D., & Satz, P.Superiority of right visual half-fields in right handers for recall of digits presented at varying rates. Neuropsychologia. 9:21–25. 1971.CrossRefGoogle ScholarPubMed
Hudson, P. T. W.The genetics of handedness - a reply to Levy and Nagylaki. Neuropsychologia. 13:331–39. 1975.CrossRefGoogle Scholar
Hummel, K. P., & Chapman, D. B.Visceral asymmetry and associated anomalies in the mouse. Journal of Heredity. 50:9–13. 1959.CrossRefGoogle Scholar
Layton, W. M. Jr., Random determination of a developmental process. Journal of Heredity. 67:336–38. 1976.CrossRefGoogle ScholarPubMed
Lepori, N. G.Sur la genèse des structures asymetriques chez l'embryon des oiseaux. Monitore Zoologico Italiano. 3:33–53. 1969.Google Scholar
Lerner, I. M.Genetic homeostasis. Edinburgh: Oliver & Boyd, 1954.Google Scholar
Levy, J. The origins of lateral asymmetry. In: Hamad, S. R., Doty, R. W., Goldstein, L., Jaynes, J., & Krauthamer, G. (eds.), Lateralization in the nervous system. New York: Academic Press, 1977.Google Scholar
Levy, J., & Nagylaki, T.A model for the genetics of handedness. Genetics. 72:117–28. 1972.CrossRefGoogle Scholar
Lindsley, D. L., & Grell, E. H.The genetic variations of Drosophila melanogaster. Washington, D.C.: The Carnegie Institute, Publication No. 627, 1967.Google Scholar
Marengo, N. P., & Howland, R. B.The effect of the gene abdomen rotation on the development of Drosophila melanogaster. Genetics. 27:604–11. 1942.CrossRefGoogle Scholar
Milner, B. Psychological aspects of focal epilepsy and its neurosurgical management. In: Purpura, D. P., Penry, J. K., & Walter, R. D. (eds.), Advances in neurology, Vol. 8. New York: Raven Press, 1975.Google Scholar
Milner, B., Branch, C., & Rasmussen, T. Observations on cerebral dominance. In: de Reuck, A. V. S. & O'Connor, M. (eds.), Ciba symposium on disorders of language. London: Churchill, 1964.Google Scholar
Morgan, M. J. Embryology and inheritance of asymmetry. In: Harnad, S. R., Doty, R. W., Goldstein, L., Jaynes, J., & Krauthamer, G. (eds.), Lateralization in the nervous system. New York: Academic Press, 1977.Google Scholar
Nagylaki, T., & Levy, J.“The sound of one paw clapping” isn't sound. Behavior Genetics. 3:279–92. 1973.CrossRefGoogle ScholarPubMed
Needham, R. (ed.) Right and left: Essays on dual symbolic classification. Chicago: University of Chicago Press, 1973.Google Scholar
Peterson, G. M.Mechanisms of handedness in the rat. Comparative Psychology Monographs. 9:No. 46. 1934.Google Scholar
Plunkett, C. R.The interaction of genetic and environmental factors in development. Journal of Experimental Zoology. 46:181–244. 1926.CrossRefGoogle Scholar
Ramaley, F.Inheritance of left-handedness. American Naturalist. 47:730–38. 1913.CrossRefGoogle Scholar
Rasmussen, T., & Milner, B. Clinical and surgical studies of the cerebral speech areas in man. In: Zulch, K. J., Creutzfeldt, O., & Galbraith, G. C. (eds.), Cerebral localization. Berlin: Springer-Verlag, 1975.Google Scholar
Rife, D. C.Handedness, with special reference to twins. Genetics. 25:178–86. 1940.CrossRefGoogle ScholarPubMed
Rife, D. C.Application of gene frequency analysis to the interpretation of data from twins. Human Biology. 22:136–45. 1950.Google Scholar
Rossi, G. F., & Rosadini, G. Experimental analysis of cerebral dominance in man. In: Millikan, C. H. & Darley, F. L. (eds.), Brain mechanisms underlying speech and language. New York: Grane & Stratton, 1967.Google Scholar
Satz, P.Pathological left-handedness: An explanatory model. Cortex. 8:121–35. 1972.CrossRefGoogle ScholarPubMed
Schnall, B. S., & Smith, D. W.Nonrandom laterality of malformation in paired structures. Pediatrics. 85:509–11. 1974.Google ScholarPubMed
Spemann, H., & Falkenberg, H.Uber asymmetrische Entwicklung und Situs inversus bei Zwillingen und Doppelbildungen. Wilhelm Roux Archiv für Entwicklungsmechanik. 45:371–422. 1919.CrossRefGoogle Scholar
Stern, C. Gene action. In: Willier, B. H., Weiss, P. A., & Hamburger, V. (eds.), Analysis of development. New York: Hafner Publishing Co., 1971. (Facsimile of 1955 edition.)Google Scholar
Sturtevant, A. H.Inheritance of direction of coiling in Limnaea. Science. 58:269. 1923.CrossRefGoogle Scholar
Thoday, J. M.Homeostasis in a selection experiment. Heredity. 12:401–15. 1958.CrossRefGoogle Scholar
Trankell, A.Aspects of genetics in psychology. American Journal of Human Genetics. 7:264–76. 1955.Google ScholarPubMed
Ubbels, G. A., Bezem, J. J., & Raven, C. P.Analysis of follicle cell patterns in dextral and sinistral Limnaea peragra. Journal of Embryology & Experimental Morphology. 21:445–66. 1969.Google Scholar
Wada, J., & Rasmussen, T.Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance: Experimental and clinical observations. Journal of Neurosurgery. 17:266–82. 1960.CrossRefGoogle Scholar
Warren, J. M.In discussion of paper session on “Functional Lateralization of the Brain.”Conference on Evolution and Lateralization of the Brain, New York Academy of Sciences,New York,October, 1976.CrossRefGoogle Scholar
Warrington, E. K., & Pratt, R. T. C.Language laterality in left handers assessed by unilateral ECT. Neuropsychologia. 11:423–28. 1973.CrossRefGoogle Scholar
Wilson, J. G., Jordan, H. C., & Brent, R. L.Effects of irradiation on embryonic development. American Journal of Anatomy. 92:153–87. 1953.CrossRefGoogle ScholarPubMed
Wolpert, L.Positional information and the spatial pattern of cellular differentiation. Journal of Theoretical Biology. 1–47. 1969.CrossRefGoogle ScholarPubMed
Zangwill, O. L.Cerebral dominance and its relation to psychological function. Edinburgh: Oliver & Boyd, 1960.Google Scholar
Zangwill, O. L.Thought and the brain. British J ournal of Psychology. 67:301–14. 1976.CrossRefGoogle ScholarPubMed
Zurif, E. B., & Bryden, M. P.Familial handedness and left-right differentiation in auditory and visual perception. Neuropsychologia. 7:179–87. 1969.CrossRefGoogle Scholar