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The Ontogeny of Cerebral Language Dominance
Brain and Language 71, 217–220 (2000) doi:10.1006/brln.1999.2253, available online at http://www.idealibrary.com on
The Ontogeny of Cerebral Language Dominance Ola A. Selnes Cognitive Neurology, Meyer 222, Baltimore, Maryland
There is little doubt that the pivotal brain–language discovery of the present millennium was Pierre Paul Broca’s conclusion that language functions are lateralized to one hemisphere of the brain (Broca, 1861). Broca’s discovery has clearly stood the test of time. Converging evidence from a number of different lines of inquiry has established that the majority of adults, regardless of hand preference, have their language functions lateralized to the left hemisphere (Risse, Gates, & Fangman, 1997; Binder, Rao, Hammeke, et al., 1995). The mechanisms by which a highly complex activity such as language become lateralized to one hemisphere of a bilaterally symmetrical nervous system have received surprisingly little attention. I would propose that the answer to this question should be an important topic of investigation for the next millennium. Theories concerning the ontogeny of hemispheric language lateralization fall into two major classes. One of these assumes that the language dominant hemisphere possesses some unique quality, already present at the time of birth, that makes it more adept at handling the special demands of speech and language: ‘‘The left hemisphere in man appears to be uniquely specialized for serial, segmental, time-dependent analytic processing, which probably stems from shared tool use’’ (Bradshaw & Nettleton, 1981). Thus, during early development, language-related functions presumably migrate toward whichever of the two hemispheres appears to be most suited for the demands of the task. The other class of theories assumes that the two hemispheres are relatively equipotential for the task of handling language at birth, and that the process of lateralization toward one hemisphere evolves gradually during the early years of development. Consistent with this proposal, there is some evidence Address correspondence and reprint requests to Ola A. Selnes, Ph.D., Cognitive Neurology, Meyer 222, 600 North Wolfe Street, Baltimore, MD 21287. E-mail: [email protected]. 217 0093-934X/00 $35.00
Copyright 2000 by Academic Press All rights of reproduction in any form reserved.
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that before age 5, lesions of either hemisphere will affect language with more or less equal probability. With increasing age, only left-sided lesions cause aphasia. This suggests that the two hemispheres are equipotential from birth with respect to language capacity (Lenneberg, 1967; Brown & Jaffe, 1975). What is the mechanism whereby language functions subsequently become associated with only one of the two hemispheres? Structural imaging has confirmed anatomical asymmetries in language relevant areas that may ‘‘favor’’ the dominant hemisphere, but these data do not quite correspond with standard estimates of the prevalence of left hemisphere language dominance. Additionally, asymmetries of the planum temporale have also been demonstrated in the chimpanzee, and it thus seems less likely that there is a direct connection between anatomical asymmetries and language dominance (Gannon, Holloway, Broadfield, & Braun, 1998). Once the choice of the left or right hemisphere as the home base for language has been made, it would seem advantageous to have a mechanism to suppress mirror activity in the contralateral hemisphere during language activity. The idea that the corpus callosum may be ideally suited for this task has been around for some time (Selnes, 1974). It may also have been prematurely dismissed (Cook, 1984). Recent functional studies in humans have provided more direct evidence for an inhibitory role of the corpus callosum in language relevant cortical areas (Karbe, Herholz, Halber, & Heiss, 1998). If there is a role for the corpus callosum in the establishment of cerebral language dominance, then patients who are born without this anatomical structure might provide an opportunity for testing this hypothesis. However, patients with callosal agenesis sometimes have borderline overall intellectual functions, which makes behavioral studies difficult to interpret. The degree of callosal agenesis can range from partial to complete, and the anterior commissure may be present or absent. Criteria for interpretation of bilateral language during WADA testing also lack uniformity (Benbadis, Dinner, Chelune, Piedmonte, & Luders, 1995). Nevertheless, studies of language laterality in congenitally acallosal subjects that have been confirmed with Wada testing have found bilateral language representation (Komaba, Senda, Ohyama, et al., 1998). Information about patterns of language lateralization in neurologically normal individuals is beginning to emerge from functional MRI studies. In general, these findings appear to support previous data based on WADA testing. However, strong right hemisphere language representation may be a much more rare occurrence in neurologically intact individuals than in clinical populations (Pujol, Deus, Losilla, & Capdevila, 1999). Functional imaging techniques such as PET scanning and functional MRI have also been used in subjects with lesions of the corpus callosum or callosal agenesis. Kessler and his colleagues concluded that the absence of the telencephalic commissures results in highly individual variants of language lateralization (Kessler, Huber, Pawlik, Heiss, & Markowitsch, 1991).
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Intriguing new hypotheses re ‘‘mirror neurons’’ and their possible role in the transition between manual and vocal communication have been proposed (Rizzolatti & Arbib, 1998). This new discovery may encourage further exploration of the strong link between handedness and praxis, and details of the cerebral language representation in subjects in whom language representation is dissociated from praxis (Selnes, Rubens, Risse, & Levy, 1982; Selnes, Pestronk, Hart, & Gordon, 1991). With the help of newer imaging methods that are safe and reproducible in neurologically intact individuals, it may now be possible for the first time to sort out the complex interrelationships between handedness, motor dominance, praxis, and language dominance. An important step will be to conduct prospective, longitudinal studies from childhood through adulthood, combining measures of relative hemispheric and callosal activation, during language related tasks. As the internet is becoming a metaphor for exchange of knowledge and communication in the next millenium, the corpus callosum deserves to come into new focus as the dynamic ‘‘internet’’ of interhemispheric communication. The specific role of the corpus callosum and other commissures in language and lateralization of functions may well be different during developmental stages than in the mature brain. REFERENCES Benbadis, S. R., Dinner, D. S., Chelune, G. J., Piedmonte, M. R., & Luders, H. 1995. Objective criteria for reporting language dominance by intracarotid amobarbital procedure. Journal of Clinical and Experimental Neuropsychology, 17, 682–690. Binder, J. R., Rao, S. M., Hammeke, T. A., Frost, J. A., Bandettini, P. A., Jesmanowicz, A., & Hyde, J. S. 1995. Lateralized human brain language systems demonstrated by task subtraction functional magnetic resonance imaging. Archives of Neurology, 52, 593–601. Bradshaw, J. L., & Nettleton, N. C. 1981. The nature of hemispheric specialization in man. Behavioral Brain Sciences, 4, 51–91. Broca, P. 1861. Perte de la parole, ramollissement chronique et destruction partielle du lobe anterieure gauche du cerveau. Bulletins de la Societe d’Anthropologie de Paris, 2, 235– 238. Brown, J. W., & Jaffe, J. 1975. Hypothesis on cerebral dominance. Neuropsychologia, 13, 107–110. Cook, N. D. 1984. Callosal inhibition: The key to the brain code. Behavioral Science, 29, 98–110. Gannon, P. J., Holloway, R. L., Broadfield, D. C., & Braun, A. R. 1998. Asymmetry of chimpanzee planum temporale: Humanlike pattern of Wernicke’s brain language area homolog. Science, 279, 220–222. Karbe, H., Herholz, K., Halber, M., & Heiss, W. D. 1998. Collateral inhibition of transcallosal activity facilitates functional brain asymmetry. Journal of Cerebral Blood Flow and Metabolism, 18, 1157–1161. Kessler, J., Huber, M., Pawlik, G., Heiss, W. D., & Markowitsch, H. J. 1991. Complex sensory cross integration deficits in a case of corpus callosum agenesis with bilateral language representation: Positron-emission-tomography and neuropsychological findings. International Journal of Neuroscience, 58, 275–282.
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Komaba, Y., Senda, M., Ohyama, M., Mori, T., Ishii, K., Mishina, M., Kitamura, S., & Terashi, A. 1998. Bilateral representation of language function. Journal of Neuroimaging, 8, 246– 249. Lenneberg, E. H. 1967. Biological foundations of language. New York: Wiley. Pujol, J., Deus, J., Losilla, J. M., & Capdevila, A. 1999. Cerebral lateralization of language in normal left-handed people studied by functional MRI. Neurology, 52, 1038–1043. Risse, G. L., Gates, J. R., & Fangman, M. C. 1997. A reconsideration of bilateral language representation based on the intracarotid amobarbital procedure. Brain and Cognition, 33, 118–132. Rizzolatti, G., & Arbib, M. A. 1998. Language within our grasp. Trends in Neurosciences, 21, 188–194. Selnes, O. A. 1974. The corpus callosum: Some anatomical and functional considerations with special reference to language. Brain and Language, 1, 111–139. Selnes, O. A., Pestronk, A., Hart, J., & Gordon, B. 1991. Limb apraxia without aphasia from a left sided lesion in a right handed patient. Journal of Neurology, Neurosurgery and Psychiatry, 54, 734–737. Selnes, O. A., Rubens, A. B., Risse, G. L., & Levy, R. S. 1982. Transient aphasia with persistent apraxia: Uncommon sequela of massive left-hemisphere stroke. Archives of Neurology, 39, 122–126.
The Ontogeny of Cerebral Language Dominance Ola A. Selnes Cognitive Neurology, Meyer 222, Baltimore, Maryland
There is little doubt that the pivotal brain–language discovery of the present millennium was Pierre Paul Broca’s conclusion that language functions are lateralized to one hemisphere of the brain (Broca, 1861). Broca’s discovery has clearly stood the test of time. Converging evidence from a number of different lines of inquiry has established that the majority of adults, regardless of hand preference, have their language functions lateralized to the left hemisphere (Risse, Gates, & Fangman, 1997; Binder, Rao, Hammeke, et al., 1995). The mechanisms by which a highly complex activity such as language become lateralized to one hemisphere of a bilaterally symmetrical nervous system have received surprisingly little attention. I would propose that the answer to this question should be an important topic of investigation for the next millennium. Theories concerning the ontogeny of hemispheric language lateralization fall into two major classes. One of these assumes that the language dominant hemisphere possesses some unique quality, already present at the time of birth, that makes it more adept at handling the special demands of speech and language: ‘‘The left hemisphere in man appears to be uniquely specialized for serial, segmental, time-dependent analytic processing, which probably stems from shared tool use’’ (Bradshaw & Nettleton, 1981). Thus, during early development, language-related functions presumably migrate toward whichever of the two hemispheres appears to be most suited for the demands of the task. The other class of theories assumes that the two hemispheres are relatively equipotential for the task of handling language at birth, and that the process of lateralization toward one hemisphere evolves gradually during the early years of development. Consistent with this proposal, there is some evidence Address correspondence and reprint requests to Ola A. Selnes, Ph.D., Cognitive Neurology, Meyer 222, 600 North Wolfe Street, Baltimore, MD 21287. E-mail: [email protected]. 217 0093-934X/00 $35.00
Copyright 2000 by Academic Press All rights of reproduction in any form reserved.
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MILLENNIUM ISSUE
that before age 5, lesions of either hemisphere will affect language with more or less equal probability. With increasing age, only left-sided lesions cause aphasia. This suggests that the two hemispheres are equipotential from birth with respect to language capacity (Lenneberg, 1967; Brown & Jaffe, 1975). What is the mechanism whereby language functions subsequently become associated with only one of the two hemispheres? Structural imaging has confirmed anatomical asymmetries in language relevant areas that may ‘‘favor’’ the dominant hemisphere, but these data do not quite correspond with standard estimates of the prevalence of left hemisphere language dominance. Additionally, asymmetries of the planum temporale have also been demonstrated in the chimpanzee, and it thus seems less likely that there is a direct connection between anatomical asymmetries and language dominance (Gannon, Holloway, Broadfield, & Braun, 1998). Once the choice of the left or right hemisphere as the home base for language has been made, it would seem advantageous to have a mechanism to suppress mirror activity in the contralateral hemisphere during language activity. The idea that the corpus callosum may be ideally suited for this task has been around for some time (Selnes, 1974). It may also have been prematurely dismissed (Cook, 1984). Recent functional studies in humans have provided more direct evidence for an inhibitory role of the corpus callosum in language relevant cortical areas (Karbe, Herholz, Halber, & Heiss, 1998). If there is a role for the corpus callosum in the establishment of cerebral language dominance, then patients who are born without this anatomical structure might provide an opportunity for testing this hypothesis. However, patients with callosal agenesis sometimes have borderline overall intellectual functions, which makes behavioral studies difficult to interpret. The degree of callosal agenesis can range from partial to complete, and the anterior commissure may be present or absent. Criteria for interpretation of bilateral language during WADA testing also lack uniformity (Benbadis, Dinner, Chelune, Piedmonte, & Luders, 1995). Nevertheless, studies of language laterality in congenitally acallosal subjects that have been confirmed with Wada testing have found bilateral language representation (Komaba, Senda, Ohyama, et al., 1998). Information about patterns of language lateralization in neurologically normal individuals is beginning to emerge from functional MRI studies. In general, these findings appear to support previous data based on WADA testing. However, strong right hemisphere language representation may be a much more rare occurrence in neurologically intact individuals than in clinical populations (Pujol, Deus, Losilla, & Capdevila, 1999). Functional imaging techniques such as PET scanning and functional MRI have also been used in subjects with lesions of the corpus callosum or callosal agenesis. Kessler and his colleagues concluded that the absence of the telencephalic commissures results in highly individual variants of language lateralization (Kessler, Huber, Pawlik, Heiss, & Markowitsch, 1991).
MILLENNIUM ISSUE
219
Intriguing new hypotheses re ‘‘mirror neurons’’ and their possible role in the transition between manual and vocal communication have been proposed (Rizzolatti & Arbib, 1998). This new discovery may encourage further exploration of the strong link between handedness and praxis, and details of the cerebral language representation in subjects in whom language representation is dissociated from praxis (Selnes, Rubens, Risse, & Levy, 1982; Selnes, Pestronk, Hart, & Gordon, 1991). With the help of newer imaging methods that are safe and reproducible in neurologically intact individuals, it may now be possible for the first time to sort out the complex interrelationships between handedness, motor dominance, praxis, and language dominance. An important step will be to conduct prospective, longitudinal studies from childhood through adulthood, combining measures of relative hemispheric and callosal activation, during language related tasks. As the internet is becoming a metaphor for exchange of knowledge and communication in the next millenium, the corpus callosum deserves to come into new focus as the dynamic ‘‘internet’’ of interhemispheric communication. The specific role of the corpus callosum and other commissures in language and lateralization of functions may well be different during developmental stages than in the mature brain. REFERENCES Benbadis, S. R., Dinner, D. S., Chelune, G. J., Piedmonte, M. R., & Luders, H. 1995. Objective criteria for reporting language dominance by intracarotid amobarbital procedure. Journal of Clinical and Experimental Neuropsychology, 17, 682–690. Binder, J. R., Rao, S. M., Hammeke, T. A., Frost, J. A., Bandettini, P. A., Jesmanowicz, A., & Hyde, J. S. 1995. Lateralized human brain language systems demonstrated by task subtraction functional magnetic resonance imaging. Archives of Neurology, 52, 593–601. Bradshaw, J. L., & Nettleton, N. C. 1981. The nature of hemispheric specialization in man. Behavioral Brain Sciences, 4, 51–91. Broca, P. 1861. Perte de la parole, ramollissement chronique et destruction partielle du lobe anterieure gauche du cerveau. Bulletins de la Societe d’Anthropologie de Paris, 2, 235– 238. Brown, J. W., & Jaffe, J. 1975. Hypothesis on cerebral dominance. Neuropsychologia, 13, 107–110. Cook, N. D. 1984. Callosal inhibition: The key to the brain code. Behavioral Science, 29, 98–110. Gannon, P. J., Holloway, R. L., Broadfield, D. C., & Braun, A. R. 1998. Asymmetry of chimpanzee planum temporale: Humanlike pattern of Wernicke’s brain language area homolog. Science, 279, 220–222. Karbe, H., Herholz, K., Halber, M., & Heiss, W. D. 1998. Collateral inhibition of transcallosal activity facilitates functional brain asymmetry. Journal of Cerebral Blood Flow and Metabolism, 18, 1157–1161. Kessler, J., Huber, M., Pawlik, G., Heiss, W. D., & Markowitsch, H. J. 1991. Complex sensory cross integration deficits in a case of corpus callosum agenesis with bilateral language representation: Positron-emission-tomography and neuropsychological findings. International Journal of Neuroscience, 58, 275–282.
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Komaba, Y., Senda, M., Ohyama, M., Mori, T., Ishii, K., Mishina, M., Kitamura, S., & Terashi, A. 1998. Bilateral representation of language function. Journal of Neuroimaging, 8, 246– 249. Lenneberg, E. H. 1967. Biological foundations of language. New York: Wiley. Pujol, J., Deus, J., Losilla, J. M., & Capdevila, A. 1999. Cerebral lateralization of language in normal left-handed people studied by functional MRI. Neurology, 52, 1038–1043. Risse, G. L., Gates, J. R., & Fangman, M. C. 1997. A reconsideration of bilateral language representation based on the intracarotid amobarbital procedure. Brain and Cognition, 33, 118–132. Rizzolatti, G., & Arbib, M. A. 1998. Language within our grasp. Trends in Neurosciences, 21, 188–194. Selnes, O. A. 1974. The corpus callosum: Some anatomical and functional considerations with special reference to language. Brain and Language, 1, 111–139. Selnes, O. A., Pestronk, A., Hart, J., & Gordon, B. 1991. Limb apraxia without aphasia from a left sided lesion in a right handed patient. Journal of Neurology, Neurosurgery and Psychiatry, 54, 734–737. Selnes, O. A., Rubens, A. B., Risse, G. L., & Levy, R. S. 1982. Transient aphasia with persistent apraxia: Uncommon sequela of massive left-hemisphere stroke. Archives of Neurology, 39, 122–126.