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On the biological basis of human laterality: I. Evidence for a maturational left–right gradient

Published online by Cambridge University Press:  04 February 2010

Michael C. Corballis  and
Michael J. Morgan
Michael C. Corballis
Affiliation:
Department of Psychology, University of Auckland, Auckland, New Zealand
Michael J. Morgan
Affiliation:
Department of Psychology, University of Durham, Durham OH1 3LE England
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Abstract

In this paper, we consider human handedness and cerebral lateralization in a general biological context, and attempt to arrive at some conclusions common to the growth of human laterality and of other structural asymmetries. We suggest that many asymmetries appear to be under the influence of a left-right maturational gradient, which often seems to favor earlier or more rapid development on the left than on the right. If the leading side is damaged or restricted, this gradient may be reversed so that growth occurs with the opposite polarity. A mechanism of this sort appears to underlie the phenomenon of situs inversus viscerum et cordis, and the same principle may help explain the equipotentiality of the two sides of the human brain with respect to the representation of language in the early years of life. However we must also suppose that the leading side normally exerts an inhibitory influence on the lagging side, for otherwise one would expect language ultimately to develop in both halves of the brain. Examples of an inhibitory influence of this kind can also be found in other biological asymmetries; for instance, in the crab Alpheus heterochelis, one claw is normally greatly enlarged relative to the other, but if the larger claw is removed the smaller one is apparently released from its inhibitory influence and grows larger.

This last example is particularly interesting because it suggests a mechanism comparable to that proposed by Annett to account for the distribution of handedness in the human population. She argued, in effect, that there is a “right shift” factor among the majority of the population, but that among a minority who lack this factor handedness is determined at random. If it is supposed that cerebral lateralization is also determined at random among this recessive minority, the model can be extended to provide a reasonable fit to the data on the correlation between handedness and cerebral lateralization. However this genetic model (or any other) still fails to account for the near-binomial distribution of handedness among twins and among nontwin siblings. We suggest that right-handedness and leftcerebral dominance for language are manifestations of an underlying gradient which is probably coded in the cytoplasm rather than in the genes. We must leave open the question as to whether departures from this pattern are due to a recessive gene which effectively cancels the asymmetry to environmental influences, or to both genetic and cytoplasmic factors.

Keywords

asymmetrycerebral dominancehandednesslateralitymaturation
Type
Target Article
Information
Behavioral and Brain Sciences , Volume 1 , Issue 2 , June 1978 , pp. 261 - 269
Copyright
Copyright © Cambridge University Press 1978

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References

REFERENCES

Annett, M.The distribution of manual asymmetry. British Journal of Psychology. 63:343–58. 1972.CrossRefGoogle ScholarPubMed
Atkinson, J., & Egeth, H.Right hemisphere superiority in visual orientation matching. Canadian Journal of Psychology. 27:152–58. 1973.CrossRefGoogle ScholarPubMed
Basser, L. S.Hemiplegia of early onset and the faculty of speech with special reference to the effects of hemispherectomy. Brain. 85:427–60. 1962.CrossRefGoogle Scholar
Bever, T. G. The nature of cerebral dominance in speech behavior of the child and adult. In: Huxley, R. & Ingram, E. (eds.), Language acquisition: Models and methods. London: Academic Press, 1971.Google Scholar
Bogen, J. E.The other side of the brain I: Dysgraphia and dyscopia following cerebral commissurotomy. Bulletin of the Los Angeles Neurological Society. 34:73–105. 1969a.Google Scholar
Bogen, J. E.The other side of the brain II: An appositional mind. Bulletin of the Los Angeles Neurological Society. 34:135–62. 1969b.Google Scholar
Bogen, J. E. & Bogen, G. M.The other side of the brain III: The corpus callosum and creativity. Bulletin of the Los Angeles Neurological Society. 34:191–220. 1969.Google Scholar
Braitenberg, V., & Kemali, N.Exceptions to bilateral symmetry in the epithalamus of lower vertebrates. Journal of Comparative Neurology. 138:137–46. 1970.CrossRefGoogle ScholarPubMed
Broca, P.Sur la faculte du langage articulé. Bulletin of Social Anthropology. 6:493–94. 1865.Google Scholar
Carey, S., & Diamond, R.From piecemeal to configurational representation of faces. Science. 195:312–14. 1977.CrossRefGoogle ScholarPubMed
Carmichael, E. A.Hemispherectomy and the localization of function. Lectures on the Scientific Basis of Medicine, 3:93–103. 1953–54.Google Scholar
Chan, K. S. F., Hsu, F. K., Chan, S. T., & Chan, Y. B.Scrotal asymmetry and handedness. Journal of Anatomy. 94:543–48. 1960.Google Scholar
Chaney, R. B., & Webster, J. C.Information in certain multidimensional sounds. Journal of the Acoustical Society of America. 40:449–55. 1966.CrossRefGoogle ScholarPubMed
Cheung, T. S.A biostatistical study of the functional consistency in the reversed claws of the adult male stone crabs. Menippe mercenaria (Say). Crustaceana. 31:137–44. 1976.CrossRefGoogle Scholar
Child, C. M.Patterns and problems of development. Chicago, Ill.: University of Chicago Press, 1941.CrossRefGoogle Scholar
Chorazyna, H.Shifts in laterality in a baby chimpanzee. Neuropsychologia. 14:381–84. 1976.CrossRefGoogle Scholar
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., & Ward, R.Evidence for an asymmetry of cerebral function in mice tested for audiogenic seizures. Nature: 226:1062–63. 1970.CrossRefGoogle ScholarPubMed
Corballis, M. C., & Beale, I. L.Bilateral symmetry and behavior. Psychological Review. 77:451–64. 1970.CrossRefGoogle ScholarPubMed
Corballis, M. C., The psychology of left and right. Hillsdale, N.J.: Lawrence Erlbaum Associates, 1976.Google Scholar
Crowell, D. H., Jones, R. H., Kapuniai, L. E., & Nakagawa, J. K.Unilateral cortical activity in newborn humans: An early index of cerebral dominance? Science. 180:205–8. 1973.CrossRefGoogle ScholarPubMed
Curry, F.A comparison of left-handed and right-handed subjects on verbal and nonverbal dichotic listening tasks. Cortex. 3:343–52. 1967.CrossRefGoogle Scholar
Davidoff, J.Hemispheric sensitivity differences in the perception of colour. Quarterly Journal of Experimental Psychology. 28:387–94. 1976.CrossRefGoogle ScholarPubMed
Dennis, M., & Komi, B.Comprehension of syntax in infantile hemiplegics after cerebral hemidecortication: Left hemisphere superiority. Brain & Language. 2:472–82. 1975.CrossRefGoogle ScholarPubMed
Dennis, M., & Whitaker, H. A.Language acquisition following hemidecortication: Linguistic superiority of the left over the right hemisphere. Brain & Language. 3:404–33. 1976.CrossRefGoogle ScholarPubMed
Dimond, S. J., & Beaumont, J. G.Hemisphere function in the human brain. New York: Wiley, 1974.Google Scholar
Durnford, M., & Kimura, D.Right hemisphere specialization for depth perception reflected in visual field differences. Nature. 231:394–95. 1971.CrossRefGoogle ScholarPubMed
Eccles, J. C.The brain and the unity of conscious experience. 19th Eddington Memorial Lecture. London: Cambridge University Press, 1965.CrossRefGoogle Scholar
Eccles, J. C.The understanding of the brain. New York: McGraw-Hill, 1973.Google Scholar
Entus, A. K. Hemisphere asymmetry in processing of dichotically presented speech and nonspeech by infants. In: Segalowitz, S. J. & Gruber, F. (eds.), Language development and neurological theory. New York: Academic Press, 1977.Google Scholar
Finch, G.Chimpanzee handedness. Science. 94:117–18. 1941.CrossRefGoogle ScholarPubMed
Friedman, H., & Davis, M.Left handedness in parrots. Auk. 55:478–80. 1938.CrossRefGoogle Scholar
Gardiner, M. F., & Walter, D. O. Evidence of hemispheric specialization from infant EEG. 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
Gazzaniga, M. S., Bogen, J. E., & Sperry, R. W.Dyspraxia following division of the cerebral commissures. Archives of Neurology. 16:606–12. 1967.CrossRefGoogle ScholarPubMed
Geffen, G., Bradshaw, J. L., & Wallace, G.Interhemispheric effects on reaction time to verbal and nonverbal stimuli. Journal of Experimental Psychology. 87:415–22. 1971.CrossRefGoogle Scholar
Geffner, D. S., & Hochberg, I.Ear laterality performance of children from low and middle socioeconomic levels on a verbal dichotic listening task. Cortex. 7:193–203. 1971.CrossRefGoogle ScholarPubMed
Geschwind, N.The apraxias: Neural mechanisms of disorders of learned movement. American Scientist. 63:188–95. 1976.Google Scholar
Geschwind, N., & Levitsky, W.Human brain: Left-right asymmetries in temporal speech region. Science. 161:186–87. 1968.CrossRefGoogle ScholarPubMed
Gesell, A., & Ames, L. B.The development of handedness. Journal of Genetic Psychology. 70:155–75. 1947.Google ScholarPubMed
Goldsmith, O.A history of the earth and animated nature. Glasgow: Blackie and Son, 1862.Google Scholar
Gordon, H. W.Hemispheric asymmetries in the perception of musical chords. Cortex. 6:387–98. 1970.CrossRefGoogle ScholarPubMed
Groves, C. P., & Humphrey, N. K.Asymmetry in gorilla skulls: Evidence of lateralized brain function? Nature. 244:53–54. 1973.CrossRefGoogle ScholarPubMed
Hammer, M., & Turkewitz, G.A sensory basis for the lateral difference in the newborn infant's responses to somesthetic stimulation. Journal of Experimental Child Psychology. 18:304–12. 1974.CrossRefGoogle ScholarPubMed
Hécaen, H., & Sauguet, J.Cerebral dominance in left-handed subjects. Cortex. 7:19–48. 1971.CrossRefGoogle ScholarPubMed
Horstadius, S.Experimental embryology of echinoderms. Oxford: Clarendon, 1973.Google Scholar
Ingram, D.Cerebral speech lateralization in young children. Neuropsychologia. 13:103–6. 1975.CrossRefGoogle ScholarPubMed
Jackson, J. H.Abstract of the Goulstonian lectures on certain points in the study and classification of diseases of the nervous system. Lancet. 1:344. 1869.Google Scholar
Jacob, F., & Monod, J.Genetic regulatory mechanisms and the synthesis of proteins. Journal of Molecular Biology. 3:318–56. 1961.CrossRefGoogle ScholarPubMed
Kallman, H. J., & Corballis, M. C.Ear asymmetry in reaction time to musical sounds. Perception ir Psychophysics. 17:368–70. 1975.CrossRefGoogle Scholar
Kimura, D.Left-right differences in the perception of melodies. Quarterly Journal of Experimental Psychology. 16:355–58. 1964.CrossRefGoogle Scholar
Kimura, D.Functional asymmetry of the brain in dichotic listening. Cortex. 3:163–78. 1967.CrossRefGoogle Scholar
Kimura, D.Spatial localization in left and right visual fields. Canadian Journal of Psychology. 23:445–58. 1969.CrossRefGoogle ScholarPubMed
Kinsbourne, M., & Smith, W. L. (eds.). Hemispheric disconnection and cerebral function. Springfield, III: Charles C. Thomas, 1974.Google Scholar
Kohn, B., & Dennis, M. Patterns of hemispheric specialization after hemidecortication for infantile hemiplegia. In: Kinsbourne, M. & Smith, W. L. (eds.), Hemispheric disconnection and cerebral function. Springfield, Ill.: Charles C. Thomas, 1974.Google Scholar
Krynauw, R. A.Infantile hemiplegia treated by removing one cerebral hemisphere. Journal of Neurology, Neurosurgery, & Psychiatry. 13:243–67. 1950.CrossRefGoogle ScholarPubMed
Layton, W. M.Random determination of a developmental process: Reversal of normal visceral asymmetry in the mouse. Journal of Heredity. 67:336–38. 1976.CrossRefGoogle ScholarPubMed
LeMay, M. Cerebral asymmetries in nonhuman primates, Neanderthal man, and modern man. In: Hamad, S. R., Steklis, H. D., & Lancaster, J. B. (eds.), Origins and evolution of language and speech. Annals of the New York Academy of Sciences 280, 1976.Google Scholar
LeMay, M., & Geschwind, N.Hemispheric differences in the brains of great apes. Brain, Behavior, & Evolution. 11:48–52. 1975.CrossRefGoogle ScholarPubMed
Lemon, R. E.Nervous control of the syrinx in white-throated sparrows (Zonotrichia albicollis). Journal of Zoology, London. 71:131–40. 1973.CrossRefGoogle Scholar
Lenneberg, E.Biological foundations of language. New York: Wiley, 1967.CrossRefGoogle Scholar
Lepori, N. G.Sur la genèse des structures asymetriques chez l'embryon des oiseaux. Monitore Zoologico Italiano. 3:33–53. 1969.Google Scholar
Levy, J., & Nagylaki, T.A model for the genetics of handedness. Genetics. 72:117–28. 1972.CrossRefGoogle Scholar
Levy, J., & Trevarthen, C.Metacontrol of hemispheric function in human split-brain patients. Journal of Experimental Psychology: Human Perception & Performance: 2:229–312. 1976.Google ScholarPubMed
Milner, B.Interhemispheric differences in the localization of psychological processes in man. British Medical Bulletin. 27:272–77. 1971.CrossRefGoogle ScholarPubMed
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
Mittwoch, U. Lateral asymmetry and the function of the mammalian Y chromosome. In: Jones, K. & Brandham, P. E. (eds.), Current chromosome research. Amsterdam: North-Holland Publishing Co., 1976.Google Scholar
Mittwoch, U.To be right is to be born male. New Scientist. 73 (1034):74–76. 1917.Google Scholar
Molfese, D. L., Freeman, R. B. Jr., & Palermo, D. S.The ontogeny of brain lateralization for speech and nonspeech sounds. Brain & Language. 2:356–68. 1975.CrossRefGoogle Scholar
Morgan, M. J. Embryology and inheritance of 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
Morgan, M. J., & Corballis, M. C.Scrotal asymmetry and Rodin's dyslexia. Nature. 264:295–96. 1976.CrossRefGoogle Scholar
Morgan, M. J., O'Donnell, J. M., & Oliver, R. F.Development of left-right asymmetry in the habenular nuclei of Rana temporaria. Journal of Comparative Neurology. 149:203–14. 1973.CrossRefGoogle ScholarPubMed
Nottebohm, F.Neural lateralization of vocal control in a passerine bird. I. Song. Journal of Experimental Zoology. 177:229–62. 1971.CrossRefGoogle Scholar
Nottebohm, F.Neural lateralization of vocal control in a passerine bird. II. Subsong, calls, and a theory of vocal learning. Journal of Experimental Zoology. 179:25–50. 1972.Google Scholar
Nottebohm, F. Asymmetries in neural control of vocalization in the canary. 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
Oppenheimer, J. M.Asymmetry revisited. American Zoologist. 14:867–879. 1974.CrossRefGoogle Scholar
Peterson, G. M.Mechanisms of handedness in the rat. Comparative Psychology Mongraphs. 9, No. 46. 1934.Google Scholar
Phippard, D.Hemifield differences in visual perception in deaf and hearing subjects. Neuropsychologia. 15:555–62. 1977.CrossRefGoogle ScholarPubMed
Rife, D. C.Handedness, with special reference to twins. Genetics. 25:178–86. 1940.CrossRefGoogle ScholarPubMed
Romer, A. S.The vertebrate body. London: W. B. Saunders, 1962.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: Grune & Stratton, 1967.Google Scholar
Smith, A.Nondominant hemispherectomy. Neurology. 19:442–45. 1969.CrossRefGoogle ScholarPubMed
Spemann, H., & Falkenberg, H.Über asymmetrische Entwicklung und Situs inversus bei Zwillingen und Doppelbildungen. Wilhelm Roux Archiv für Entwicklungsmechanik. 45:371–422. 1919.CrossRefGoogle Scholar
Taylor, D. C. Differential rates of cerebral maturation between sexes and between hemispheres. Lancet. 140–42. 1969 (July 19).CrossRefGoogle Scholar
Turkewitz, G., Gordon, E. W., & Birch, H. G.Head-turning in the human neonate: Effect of prandial condition and lateral preference. Journal of Comparative & Physiological Psychology. 59:189–92. 1965.CrossRefGoogle ScholarPubMed
Turkewitz, G., Moreau, T., Birch, H. G., & Crystal, D.Relationships between prior head position and lateral differences in responsiveness to somesthetic stimulation in the human neonate. Journal of Experimental Child Psychology. 5:548–61. 1967.CrossRefGoogle ScholarPubMed
Vargha-Khadem, F., & Corballis, M. C.Cerebral asymmetry in infants.Paper presented at the Biennial Meeting of the Society for Research in Child Developmentin New Orleans, Louisiana,March, 1977.Google Scholar
von Kraft, A.Situs inversus beim Alpenmolch (Trifurus alvestris) nach UV-Bestrahlung von Gastrula-Keimen. Wilhelm Roux Archiv für Entwicklungsmechanik. 161:351–74. 1968.CrossRefGoogle Scholar
von Woellwarth, C.Experimentelle Untersuchungen über dem Situs inversus der Eingeweide und der Habenula des Zwischenhirns bei Amphibien. Wilhelm Roux Archiv für Entwicklungsmechanik. 144:178–256. 1950.CrossRefGoogle Scholar
Wada, J. A., Clarke, R., & Hamm, A.Cerebral hemispheric asymmetry in humans. Archives of Neurology. 32:239–46. 1975.CrossRefGoogle ScholarPubMed
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, 1977.CrossRefGoogle Scholar
Warren, J. M. Handedness and cerebral dominance in monkeys. 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
Wilhelmi, H.Experimentelle untersuchungen über situs inversus viscerum. Wilhelm Roux Archiv für Entwicklungsmechanik. 48:517–532. 1921.CrossRefGoogle Scholar
Wilson, E. B.Notes on the reversal of asymmetry in the regeneration of chelae in Alpheus heterochelis. Biological Bulletin (of the Marine Biological Laboratory, Woods Hole, Mass.), 4:197–210. 1903.CrossRefGoogle Scholar
Witelson, S. F.Hemispheric specialization for linguistic and nonlinguistic tactual perception using a dichotomous stimulation technique. Cortex. 10:3–17. 1974.CrossRefGoogle ScholarPubMed
Witelson, S. F.Sex and the single hemisphere: Specialization of the right hemisphere for spatial processing. Science. 193:425–27. 1976.CrossRefGoogle ScholarPubMed
Witelson, S. F., & Pallie, W.Left hemisphere specialization for language in the newborn: Neuroanatomical evidence of asymmetry. Brain. 96:641–46. 1973.CrossRefGoogle ScholarPubMed
Yeni-Komshian, G. H., & Benson, D. A.Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys. Science. 192:387–89. 1976.CrossRefGoogle ScholarPubMed
Youngren, O. M., Peek, F. W., & Phillips, R. E.Repetitive vocalizations evoked by local electrical stimulation of avian brains. Brain, Behavior, & Evolution. 9:393–421. 1974.CrossRefGoogle Scholar
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 Journal of Psychology. 67:301–14. 1976.CrossRefGoogle ScholarPubMed
Zollinger, R.Removal of left cerebral hemisphere: Report of a case. Archives of Neurology & Psychiatry. 34:1055–64. 1935.CrossRefGoogle Scholar