c o r t e x x x x ( 2 0 1 4 ) 1 e3
Available online at www.sciencedirect.com
ScienceDirect Journal homepage: www.elsevier.com/locate/cortex
Discussion forum
Praxis, language, and handedness: A tricky triad Guy Vingerhoets Department of Experimental Psychology, Ghent University, Belgium
On several occasions in his excellent monograph on apraxia, Georg Goldenberg points at the relation between apraxia, aphasia, and handedness (Goldenberg, 2013b). The cooccurrences of these manifestations are believed to shed light on their cerebral organization as well as on their mutual (in)dependence. In my comment I would like to emphasize the difficulties associated with claims regarding relations between cognitive functions and their neural correlates, in particular when it comes to their hemispheric colateralization. First I will outline the stance taken by Goldenberg, then I will provide some empirical and theoretical insights that might hint at an alternative reading of the clinical data. In several chapters the question is raised whether there exists an obligatory relation between apraxia and aphasia, as in right handers these symptoms occur most often following left hemispheric lesions. Clearly, many studies have reported a strong association between symptoms of apraxia and aphasia and their co-occurrence even increases in clinical studies that use dichotomous categorizations or focus on severe types of aphasia such as global aphasia (Duffy & Duffy, 1981; Goldenberg, Hartmann, & Schlott, 2003, Goldenberg, Hermsdorfer, Glindemann, Rorden, & Karnath, 2007; Wang & Goodglass, 1992). Although it seems from these data that most patients suffering from aphasia also tend to show apraxia, the relation is not mandatory, and dissociations are believed to be more prominent in lefthanded patients. Goldenberg devotes a separate chapter to apraxia in left handers. According to his view “the absence of right handedness leads to a reshuffling of asymmetric brain functions resulting in a random distribution of their laterality” (p. 185). This experiment of nature offers the opportunity to investigate what functions ‘go together’ and form an obligatory link, and what functions are independent. Gold-
enberg states that if two such functions “are in fact subcomponents of one overarching function, they will always be located in the same hemisphere” (p. 186). Subsequent exploration of clinical data of left-handed patients with apraxia is taken to suggest that most left-handers do not exhibit a more symmetric organization of apraxia, but reveal bilateral disturbances following unilateral lesions, just like right-handers. Goldenberg continues to demonstrate that left-handed patients suffer from apraxia as a consequence of left or right unilateral brain damage that may or may not be accompanied by aphasia (Goldenberg, 2013a, 2013b). He concludes that neither the relation between apraxia and aphasia nor between apraxia and handedness is obligatory and that “.the laterality of apraxia can vary independently from aphasia or handedness.” (p. 190). As Goldenberg elegantly demonstrates, apraxia is not a monolithic construct but consists of several (at least partially dissociated) symptoms flagging disturbances of an overarching cognitive function called praxis. The same can be said for aphasia with respect to language. In addition to the composed nature of these cognitive concepts, neuroimaging has unveiled that in normal participants tasks of praxis and language typically activate clusters of regions whose lateralization depends on the particular subcomponent and region under investigation. Handedness is a multifaceted concept too, that varies with the method of assessment and the applied categorization. Dividing individuals in right and left handers might not do justice to the complex influence of this trait, in particular when relating handedness to asymmetry of cognitive function. Very few right handers show right hemispheric language dominance, but considerably more left handers do. As a result, left handed groups are more likely to contain some individuals with atypical functional asymmetries, resulting in lower mean asymmetry scores in behavioral and functional imaging studies. Given the complexity of the
0010-9452/$ e see front matter ª 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cortex.2014.01.019
Please cite this article in press as: Vingerhoets, G., Praxis, language, and handedness: A tricky triad, Cortex (2014), http:// dx.doi.org/10.1016/j.cortex.2014.01.019
2
c o r t e x x x x ( 2 0 1 4 ) 1 e3
concepts of apraxia, aphasia, and handedness, a dichotomous comparison of its manifestations is tricky. I want to illustrate this point further with some recent insights from neuroimaging on the relation between praxis, language, and handedness. One study explored the cerebral activation during the pantomiming of tool use in healthy right and left handed participants (Vingerhoets et al., 2012). The groups were matched for strength of handedness. Participants executed the pantomimes with their dominant and nondominant hand, thus making abstraction of the hand performing the task. A left lateralized activation pattern of dorsolateral prefrontal, dorsal and ventral premotor, and superior and inferior parietal cortex was found that was similar in the right and the left handed group. Only when the lateralization index of separate regions was calculated, left handers revealed significantly less asymmetric activation in the parietal areas. A second study investigated the neural response during the same pantomime paradigm in participants with known typical and atypical language dominance (Vingerhoets et al., 2013). The volunteers were matched for strength and direction of handedness. In addition to pantomiming the use of tools they also performed a word production task. Results revealed that the gesture and word production tasks activated both separate and common areas in dorsolateral prefrontal, ventral and dorsal premotor, supplementary motor, and posterior parietal cortex. In addition, it appeared that participants with typical language dominance showed a leftward asymmetry for tool pantomiming and word generation, whereas the atypical group disclosed a right hemispheric pattern for these tasks. The asymmetry could be demonstrated at the individual level and showed no exceptions, that is, typical language dominant volunteers always revealed left lateralized praxis patterns and all atypical language dominant participants displayed a right hemispheric lateralization for praxis. Another recent study in participants with atypical language dominance uncovered that all of them demonstrated left hemispheric dominance for spatial attention, which is a classical right hemispheric function in typical language dominant individuals (Cai, Van der Haegen, & Brysbaert, 2013). Together, the neuroimaging data suggest that (1) hand preference is not related to the side of lateralization of the praxis network, and (2) that atypical brain organization is commonly expressed as a mirrored, rather than a randomized distribution of functions with praxis and language residing in the same hemisphere and spatial attention preferring the opposite side. Several scholars have hypothesized a gestural origin of language to explain the intimate and perhaps evolutionary link between language and praxis and even proposed that the neural correlates of proto-speech may have evolved from a proto-sign system (Arbib, 2005, 2006; Corballis, 2002). This common neural origin hypothesis is not incompatible with Goldenberg’s assumption of an anatomical grounding of segmentation and combination as central features subserving language and meaningful manual action. If these elements are indeed reflected in structural properties of the brain as suggested by Goldenberg, and if “.segmentation and combination depend on the anatomical properties of strictly lateralized brain functions.” (p. 228), then it is also reasonable to assume that a more efficient brain organization would be to place similar functions in
neighboring parts of the same hemisphere, rather than to duplicate a similar system in two hemispheres. In the light of these empirical and theoretical considerations, I’m inclined to accept the existence of a very intimate, perhaps even obligatory link between praxis and language. The question remains whether the clinical data of the left handed patients presented by Goldenberg can be explained while assuming that in most people praxis and language are likely confined to the same hemisphere. I believe they can. If we assume that language and praxis occupy neighboring and sometimes even overlapping neural regions within the same hemisphere, it becomes likely that the average lesion will result in disturbances of praxis and language. Large lesions giving rise to global aphasia or severe apraxia will almost automatically impact both functions, but smaller lesions that remain limited to language-only or praxis-only areas may demonstrate themselves as aphasia without apraxia or apraxia without aphasia while both functions may still be lateralized in the same hemisphere. If left handers have an increased likelihood of atypical language dominance, then a higher occurrence of aphasia, apraxia, or both following right hemispheric lesions in left handers is to be expected, although the majority would still show this clinical picture upon left brain damage. The differential co-occurrence of aphasia with different types of gestures can be explained by assuming that some manifestations of praxis have a higher overlap with language than others, which might give rise to the higher correlation of pantomiming (portrayed in the monograph as an essentially communicative gesture) with defective language. Whilst I would not disagree with many of the views articulated in this book, I’m less convinced of the assertion that there is no obligatory link between praxis and language in the sense that each function can be expressed in a different hemisphere in the same individual. At the same time, I am completely convinced about the importance of this magnificent monograph for the study of apraxia and praxis, and I especially value its scholarly and neuropsychological approach. Following up on the tradition of his compatriot Hugo Karl Liepmann some 100 years ago, Georg Goldenberg has provided us with enough ideas and insights to entertain another century of research on the cognitive side of motor control.
references
Arbib, M. A. (2005). From monkey-like action recognition to human language: an evolutionary framework for neurolinguistics. Behavioral and Brain Sciences, 28, 105e167. Arbib, M. A. (2006). Aphasia, apraxia and the evolution of the language-ready brain. Aphasiology, 20, 1125e1155. Cai, Q., Van der Haegen, L., & Brysbaert, M. (2013). Complementary hemispheric specialization for language production and visuospatial attention. Proceedings of the National Academy of Sciences of the United States of America, 110, E322eE330. Corballis, M. C. (2002). From hand to mouth: The origins of language. Princeton, NJ: Princeton University Press. Duffy, R. J., & Duffy, J. R. (1981). Three studies of deficits in pantomimic expression and pantomimic recognition in aphasia. Journal of Speech and Hearing Research, 14, 70e84.
Please cite this article in press as: Vingerhoets, G., Praxis, language, and handedness: A tricky triad, Cortex (2014), http:// dx.doi.org/10.1016/j.cortex.2014.01.019
c o r t e x x x x ( 2 0 1 4 ) 1 e3
Goldenberg, G. (2013a). Apraxia in left-handers. Brain, 136, 2592e2601. Goldenberg, G. (2013b). Apraxia. The cognitive side of motor control. Oxford: Oxford University Press. Goldenberg, G., Hartmann, K., & Schlott, I. (2003). Defective pantomime of object use in left brain damage: apraxia or asymbolia? Neuropsychologia, 41, 1565e1573. Goldenberg, G., Hermsdorfer, J., Glindemann, R., Rorden, C., & Karnath, H. O. (2007). Pantomime of tool use depends on integrity of left inferior frontal cortex. Cerebral Cortex, 17, 2769e2776. Vingerhoets, G., Acke, F., Alderweireldt, A. S., Nys, J., Vandemaele, P., & Achten, E. (2012). Cerebral lateralization of
3
praxis in right- and left-handedness: same pattern, different strength. Human Brain Mapping, 33, 763e777. Vingerhoets, G., Alderweireldt, A. S., Vandemaele, P., Cai, Q., Van der Haegen, L., Brysbaert, M., et al. (2013). Praxis and language are linked: evidence from co-lateralization in individuals, with atypical language dominance. Cortex, 49, 172e183. Wang, L. Z., & Goodglass, H. (1992). Pantomime, praxis, and aphasia. Brain and Language, 42, 402e418.
Received 22 January 2014 Accepted 23 January 2014
Please cite this article in press as: Vingerhoets, G., Praxis, language, and handedness: A tricky triad, Cortex (2014), http:// dx.doi.org/10.1016/j.cortex.2014.01.019
Available online at www.sciencedirect.com
ScienceDirect Journal homepage: www.elsevier.com/locate/cortex
Discussion forum
Praxis, language, and handedness: A tricky triad Guy Vingerhoets Department of Experimental Psychology, Ghent University, Belgium
On several occasions in his excellent monograph on apraxia, Georg Goldenberg points at the relation between apraxia, aphasia, and handedness (Goldenberg, 2013b). The cooccurrences of these manifestations are believed to shed light on their cerebral organization as well as on their mutual (in)dependence. In my comment I would like to emphasize the difficulties associated with claims regarding relations between cognitive functions and their neural correlates, in particular when it comes to their hemispheric colateralization. First I will outline the stance taken by Goldenberg, then I will provide some empirical and theoretical insights that might hint at an alternative reading of the clinical data. In several chapters the question is raised whether there exists an obligatory relation between apraxia and aphasia, as in right handers these symptoms occur most often following left hemispheric lesions. Clearly, many studies have reported a strong association between symptoms of apraxia and aphasia and their co-occurrence even increases in clinical studies that use dichotomous categorizations or focus on severe types of aphasia such as global aphasia (Duffy & Duffy, 1981; Goldenberg, Hartmann, & Schlott, 2003, Goldenberg, Hermsdorfer, Glindemann, Rorden, & Karnath, 2007; Wang & Goodglass, 1992). Although it seems from these data that most patients suffering from aphasia also tend to show apraxia, the relation is not mandatory, and dissociations are believed to be more prominent in lefthanded patients. Goldenberg devotes a separate chapter to apraxia in left handers. According to his view “the absence of right handedness leads to a reshuffling of asymmetric brain functions resulting in a random distribution of their laterality” (p. 185). This experiment of nature offers the opportunity to investigate what functions ‘go together’ and form an obligatory link, and what functions are independent. Gold-
enberg states that if two such functions “are in fact subcomponents of one overarching function, they will always be located in the same hemisphere” (p. 186). Subsequent exploration of clinical data of left-handed patients with apraxia is taken to suggest that most left-handers do not exhibit a more symmetric organization of apraxia, but reveal bilateral disturbances following unilateral lesions, just like right-handers. Goldenberg continues to demonstrate that left-handed patients suffer from apraxia as a consequence of left or right unilateral brain damage that may or may not be accompanied by aphasia (Goldenberg, 2013a, 2013b). He concludes that neither the relation between apraxia and aphasia nor between apraxia and handedness is obligatory and that “.the laterality of apraxia can vary independently from aphasia or handedness.” (p. 190). As Goldenberg elegantly demonstrates, apraxia is not a monolithic construct but consists of several (at least partially dissociated) symptoms flagging disturbances of an overarching cognitive function called praxis. The same can be said for aphasia with respect to language. In addition to the composed nature of these cognitive concepts, neuroimaging has unveiled that in normal participants tasks of praxis and language typically activate clusters of regions whose lateralization depends on the particular subcomponent and region under investigation. Handedness is a multifaceted concept too, that varies with the method of assessment and the applied categorization. Dividing individuals in right and left handers might not do justice to the complex influence of this trait, in particular when relating handedness to asymmetry of cognitive function. Very few right handers show right hemispheric language dominance, but considerably more left handers do. As a result, left handed groups are more likely to contain some individuals with atypical functional asymmetries, resulting in lower mean asymmetry scores in behavioral and functional imaging studies. Given the complexity of the
0010-9452/$ e see front matter ª 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cortex.2014.01.019
Please cite this article in press as: Vingerhoets, G., Praxis, language, and handedness: A tricky triad, Cortex (2014), http:// dx.doi.org/10.1016/j.cortex.2014.01.019
2
c o r t e x x x x ( 2 0 1 4 ) 1 e3
concepts of apraxia, aphasia, and handedness, a dichotomous comparison of its manifestations is tricky. I want to illustrate this point further with some recent insights from neuroimaging on the relation between praxis, language, and handedness. One study explored the cerebral activation during the pantomiming of tool use in healthy right and left handed participants (Vingerhoets et al., 2012). The groups were matched for strength of handedness. Participants executed the pantomimes with their dominant and nondominant hand, thus making abstraction of the hand performing the task. A left lateralized activation pattern of dorsolateral prefrontal, dorsal and ventral premotor, and superior and inferior parietal cortex was found that was similar in the right and the left handed group. Only when the lateralization index of separate regions was calculated, left handers revealed significantly less asymmetric activation in the parietal areas. A second study investigated the neural response during the same pantomime paradigm in participants with known typical and atypical language dominance (Vingerhoets et al., 2013). The volunteers were matched for strength and direction of handedness. In addition to pantomiming the use of tools they also performed a word production task. Results revealed that the gesture and word production tasks activated both separate and common areas in dorsolateral prefrontal, ventral and dorsal premotor, supplementary motor, and posterior parietal cortex. In addition, it appeared that participants with typical language dominance showed a leftward asymmetry for tool pantomiming and word generation, whereas the atypical group disclosed a right hemispheric pattern for these tasks. The asymmetry could be demonstrated at the individual level and showed no exceptions, that is, typical language dominant volunteers always revealed left lateralized praxis patterns and all atypical language dominant participants displayed a right hemispheric lateralization for praxis. Another recent study in participants with atypical language dominance uncovered that all of them demonstrated left hemispheric dominance for spatial attention, which is a classical right hemispheric function in typical language dominant individuals (Cai, Van der Haegen, & Brysbaert, 2013). Together, the neuroimaging data suggest that (1) hand preference is not related to the side of lateralization of the praxis network, and (2) that atypical brain organization is commonly expressed as a mirrored, rather than a randomized distribution of functions with praxis and language residing in the same hemisphere and spatial attention preferring the opposite side. Several scholars have hypothesized a gestural origin of language to explain the intimate and perhaps evolutionary link between language and praxis and even proposed that the neural correlates of proto-speech may have evolved from a proto-sign system (Arbib, 2005, 2006; Corballis, 2002). This common neural origin hypothesis is not incompatible with Goldenberg’s assumption of an anatomical grounding of segmentation and combination as central features subserving language and meaningful manual action. If these elements are indeed reflected in structural properties of the brain as suggested by Goldenberg, and if “.segmentation and combination depend on the anatomical properties of strictly lateralized brain functions.” (p. 228), then it is also reasonable to assume that a more efficient brain organization would be to place similar functions in
neighboring parts of the same hemisphere, rather than to duplicate a similar system in two hemispheres. In the light of these empirical and theoretical considerations, I’m inclined to accept the existence of a very intimate, perhaps even obligatory link between praxis and language. The question remains whether the clinical data of the left handed patients presented by Goldenberg can be explained while assuming that in most people praxis and language are likely confined to the same hemisphere. I believe they can. If we assume that language and praxis occupy neighboring and sometimes even overlapping neural regions within the same hemisphere, it becomes likely that the average lesion will result in disturbances of praxis and language. Large lesions giving rise to global aphasia or severe apraxia will almost automatically impact both functions, but smaller lesions that remain limited to language-only or praxis-only areas may demonstrate themselves as aphasia without apraxia or apraxia without aphasia while both functions may still be lateralized in the same hemisphere. If left handers have an increased likelihood of atypical language dominance, then a higher occurrence of aphasia, apraxia, or both following right hemispheric lesions in left handers is to be expected, although the majority would still show this clinical picture upon left brain damage. The differential co-occurrence of aphasia with different types of gestures can be explained by assuming that some manifestations of praxis have a higher overlap with language than others, which might give rise to the higher correlation of pantomiming (portrayed in the monograph as an essentially communicative gesture) with defective language. Whilst I would not disagree with many of the views articulated in this book, I’m less convinced of the assertion that there is no obligatory link between praxis and language in the sense that each function can be expressed in a different hemisphere in the same individual. At the same time, I am completely convinced about the importance of this magnificent monograph for the study of apraxia and praxis, and I especially value its scholarly and neuropsychological approach. Following up on the tradition of his compatriot Hugo Karl Liepmann some 100 years ago, Georg Goldenberg has provided us with enough ideas and insights to entertain another century of research on the cognitive side of motor control.
references
Arbib, M. A. (2005). From monkey-like action recognition to human language: an evolutionary framework for neurolinguistics. Behavioral and Brain Sciences, 28, 105e167. Arbib, M. A. (2006). Aphasia, apraxia and the evolution of the language-ready brain. Aphasiology, 20, 1125e1155. Cai, Q., Van der Haegen, L., & Brysbaert, M. (2013). Complementary hemispheric specialization for language production and visuospatial attention. Proceedings of the National Academy of Sciences of the United States of America, 110, E322eE330. Corballis, M. C. (2002). From hand to mouth: The origins of language. Princeton, NJ: Princeton University Press. Duffy, R. J., & Duffy, J. R. (1981). Three studies of deficits in pantomimic expression and pantomimic recognition in aphasia. Journal of Speech and Hearing Research, 14, 70e84.
Please cite this article in press as: Vingerhoets, G., Praxis, language, and handedness: A tricky triad, Cortex (2014), http:// dx.doi.org/10.1016/j.cortex.2014.01.019
c o r t e x x x x ( 2 0 1 4 ) 1 e3
Goldenberg, G. (2013a). Apraxia in left-handers. Brain, 136, 2592e2601. Goldenberg, G. (2013b). Apraxia. The cognitive side of motor control. Oxford: Oxford University Press. Goldenberg, G., Hartmann, K., & Schlott, I. (2003). Defective pantomime of object use in left brain damage: apraxia or asymbolia? Neuropsychologia, 41, 1565e1573. Goldenberg, G., Hermsdorfer, J., Glindemann, R., Rorden, C., & Karnath, H. O. (2007). Pantomime of tool use depends on integrity of left inferior frontal cortex. Cerebral Cortex, 17, 2769e2776. Vingerhoets, G., Acke, F., Alderweireldt, A. S., Nys, J., Vandemaele, P., & Achten, E. (2012). Cerebral lateralization of
3
praxis in right- and left-handedness: same pattern, different strength. Human Brain Mapping, 33, 763e777. Vingerhoets, G., Alderweireldt, A. S., Vandemaele, P., Cai, Q., Van der Haegen, L., Brysbaert, M., et al. (2013). Praxis and language are linked: evidence from co-lateralization in individuals, with atypical language dominance. Cortex, 49, 172e183. Wang, L. Z., & Goodglass, H. (1992). Pantomime, praxis, and aphasia. Brain and Language, 42, 402e418.
Received 22 January 2014 Accepted 23 January 2014
Please cite this article in press as: Vingerhoets, G., Praxis, language, and handedness: A tricky triad, Cortex (2014), http:// dx.doi.org/10.1016/j.cortex.2014.01.019
