ReviewHemispheric specialization for language
Introduction
Functional differences between the two cerebral hemispheres were observed from the very outset of research in neuropsychology. Marc Dax, Gustave Dax and Paul Broca (1865) showed that left-sided lesions caused aphasia more frequently than right ones [18]. These studies led to the concept of hemispheric “dominance” or “specialization”, thereby designating the better aptitude of one hemisphere as compared to the other for a given cognitive function. This aspect of cerebral organization does not concern language only, although knowledge about hemispheric specialization is more established in that case.
Broca's studies stressed the point that not all subjects have left hemispheric specialization for language. He offered a rule (named after him) defining an association between the dominant hand and the dominant hemisphere for language. According to this rule, in right-handers, the left hemisphere would be in charge of language while in left-handers, the right hemisphere would be dominant for the same function. Since then, this rule has been proved to be false, the relationship between manual preference and hemispheric specialization for language being more complex [38]. Furthermore, other variables than handedness have been found to be related to the inter-individual variability of hemispheric specialization for language, noticeably gender [38].
Studies of anatomical asymmetries between the cerebral hemispheres were also initiated in the 19th century [36]. However, it is not until 1968 that this field gained a widespread interest from researchers investigating the neural basis of language. That year, Geschwind and Levitsky [27] reported an anatomical asymmetry of the posterior sylvian region in favor of the left. This result led to the hypothesis that anatomical asymmetries were a reflection of the functional specialization of each hemisphere.
All these seminal works on hemispheric specialization were done on patients and/or postmortem brains, raising questions about the facts in healthy subjects [58], [91]. Nowadays, new methods permit the in vivo comparison of the hemispheres in healthy subjects, at both anatomical and functional levels. Particularly, magnetic resonance imaging (MRI) and positron emission tomography (PET) are of importance because of the good spatial resolution they supply. MRI allows for the study of anatomical asymmetries [76], [79], [88]. PET and functional MRI (fMRI) as well as functional transcranial Doppler ultrasonography (fTCD) permit the study of brain (de)activations in normals with a signal based on the hemodynamic response by comparing a cognitive task to a control condition. These methods can be used to investigate functional asymmetries by comparing (de)activations between the hemispheres [9], [61], [70]. While PET and fMRI can provide high-resolution whole-brain images, fTCD only gives a measure of cerebral blood flow velocity in the middle cerebral artery but its simplicity allows an easy investigation of large samples of subjects [17].
A wealth of information is being collected with these modern techniques which are encouraging new researches on hemispheric specialization [42], [57], [82]. Theories about the origins of hemispheric specialization have been built or tested, thanks to neuroimaging experiments [47], [85], [93]. These models are often not limited to language. In fact, hemispheric specializations for language on one hand and for spatial functions or music on the other hand seem not to be independent [38], [50], [93]. Thus, understanding hemispheric specialization for language in a better way should provide important clues to brain organization in general.
In this review, we first present some models of the origins of hemispheric specialization, focusing on language. Without being exhaustive, this description aims at giving an idea of the most influential hypotheses. As inter-individual variability lies at the center of most studies on hemispheric specialization for language, the second part of this review is about studies of this variability at both anatomical and functional levels. Emphasis has been put on the contributions of modern imaging techniques. The facts supplied by these studies were put in relation with the proposed origins of hemispheric specialization.
Section snippets
Genetic factors and evolution
Notwithstanding the difficulty of gathering both genetic and neurofunctional information in the same subjects, genetic models of hemispheric specialization for language already exist. Associated to the latter, handedness is more accessible to measurements and, therefore, its study has played an important part in developing these genetic models. Annett [4], [5] offered a theory based on studies of handedness and aphasia, in which the influence of the genome on hemispheric specialization is only
Clinical studies
The available data on the relationships between manual preference and hemispheric specialization were essentially supplied by clinical studies, some of which were based on several hundreds cases. A consensus admits that variability is more important in left-handers [37], [38] (for the sake of simplicity, this term will be used here to describe all non-right-handed persons, including both ambidexters and extreme left-handers). Those studies showed essentially a link between right manual
Conclusion
Allowing for in vivo studies of lateralization, the use of imaging techniques is significantly improving views about hemispheric specialization for language. It is confirming that hemispheric specialization is a complex trait varying in normals in relation to different factors like handedness and gender, as well as language tasks and brain regions. The neuroimaging findings presented here concur with the view that it is important to take into consideration several language components and brain
Acknowledgements
The authors wish to thank Petros Tzourio for translating the manuscript as well as Pierre-Yves Hervé, Gaël Jobard, Bernard Mazoyer, Laure Zago and two anonymous reviewers for helpful comments on the manuscript. Goulven Josse is supported by a grant from the Commissariat à l'Energie Atomique (CEA) and the Région Basse-Normandie, France.
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