Elsevier

Brain Research

Volume 1068, Issue 1, 12 January 2006, Pages 184-193
Brain Research

Research Report
Hemispheric specialization for language: Brain volume matters

https://doi.org/10.1016/j.brainres.2005.11.037Get rights and content

Abstract

Increasing brain volume may impose constraints, through longer information transfer delays, on the distributed networks supporting language. Here, we assessed the relative effects of brain volume and other putative predictors of the functional variability of perisylvian language areas, as probed with PET, during both a language comprehension and a language production task. In the case of language comprehension (story listening), a linear combination of planum temporale surface, brain volume and handedness could explain almost 60% of the functional asymmetry observed in the perisylvian area. Without brain volume, the goodness of fit was significantly decreased (39%, P < 0.05), and furthermore, the effect of handedness was not detected anymore. This was due to the fact that in our sample, left-handers (n = 12) had a significantly larger brain volume as compared to right-handers (n = 8, P = 0.03). As for language production (verb generation), brain volume and the planum temporale also played a role. However, in this case, the main predictor of functional variability was handedness, where a greater degree of right-handedness was associated with larger activation of left inferior frontal regions. Depending on the language component of interest, these results support different (yet compatible) theories on hemispheric specialization. Left specialization for comprehension could be attributed to the constraints of processing speech stimuli, while a gestural origin of language is mostly supported by the relation we observed between left specialization for production and right-handedness.

Introduction

The developmental and evolutionary origins of hemispheric specialization for language are still a matter of debate, but several factors are known or supposed to relate to the hemispheric specialization for speech in normal subjects. A first factor is handedness. Left-handedness is associated with a lower frequency of the left hemispheric specialization for speech typically observed in right-handers (60–70% for the higher estimates against at least 90% in right-handers, for a review, see Josse and Tzourio-Mazoyer, 2004). This relationship may be the consequence of a specific evolutionary scenario, in which a precursor of Broca's area was involved in the observation and imitation of manual movements, as well as in the understanding of actions and manual gestures performed by others (Corballis, 2003, Kohler et al., 2002, Rizzolatti and Arbib, 1998). Interestingly, Szaflarski et al. reported that handedness better explained the functional variability of frontal rather than temporal regions (Szaflarski et al., 2002). Secondly, the macro- and microscopic leftward asymmetries of the planum temporale (PT), a roughly triangular structure made of auditory cortex and found at the posterior end of the upper face of the superior temporal gyrus, have made it a possible anatomical correlate of hemispheric specialization for language (Galaburda et al., 1987, Geschwind and Levitsky, 1968, Josse and Tzourio-Mazoyer, 2004, Shapleske et al., 1999). Subsequent work has shown that the asymmetry of the PT itself was not necessarily the relevant factor (Mazoyer and Tzourio-Mazoyer, 2004). As a matter of fact, the left PT surface area, and not its asymmetry, correlated with cerebral blood flow in several areas during a speech comprehension task (Josse et al., 2003, Tzourio et al., 1998). This relation could be due to specific tuning of the left auditory cortex, including the planum temporale, for temporal processing of rapidly varying acoustic cues (Anderson et al., 1999, Golestani et al., 2002, Zatorre et al., 2002). Indeed, this type of acoustic processing is supposedly needed to properly perceive speech sounds (Tallal, 2004). Hence, during development, this specialization of the left auditory cortex could induce the specialization of higher level language regions in the same hemisphere. There is another hypothesis that relates anatomy, namely brain volume, to the relationship between the temporal aspects of speech perception and hemispheric specialization for language. It has been argued that a larger brain volume is accompanied by an increase in transfer delays especially between the hemispheres. This would favor the processing of information intra-hemispherically, thus causing hemispheric specializations (Anderson, 1999, Ringo et al., 1994). The finding of a positive relationship between both of these anatomical variables and leftward lateralization would thus support the claim that hemispheric specialization for language stems from the constraints of temporal acoustic processing (Schwartz and Tallal, 1980, Zatorre et al., 2002).

Another aspect to take into account in the study of hemispheric specialization is the language task, as well as the brain regions that are relatively specifically associated with it. A distinction notably exists between language production and comprehension tasks. Although their neural bases are largely overlapping (Papathanassiou et al., 2000), production tasks mostly activate the inferior frontal and precentral gyri, whereas the superior and middle temporal gyri constitute a major substrate of comprehension tasks. Hemispheric specialization for speech comprehension and production are usually similar but can be dissociated in some individuals (Tzourio-Mazoyer et al., 2004). This suggests that the language task is another factor among determinants of hemispheric specialization. More specifically, it is possible that determinants of hemispheric specialization differ between comprehension and production tasks. This could explain a result of our previous study in which although the left PT surface was a marker of left hemispheric specialization for speech comprehension, we could not evidence any effect of handedness (Josse et al., 2003). One reason for this may be that relevant variables, notably brain volume, were not controlled for. However, a second possibility is that handedness, because it is a measure of motor laterality, is more related to functional lateralization during production tasks than during comprehension tasks (Szaflarski et al., 2002).

Therefore, we reanalyzed the data (Josse et al., 2003) with a new regression model including as factors not only the left and right PT surfaces and handedness but also brain volume. In addition, we used this new model in the same 20 subjects to analyze the neural bases of verb generation, a production task that may be more related to handedness.

Section snippets

Behavioral data

The mean comprehension score over 17 subjects was 3.9 ± 0.6 (ranging 2.8–4.7), out of 5, showing that the subjects had paid attention to the stories (Josse et al., 2003). No significant difference was found between the comprehension scores of right- and left-handers (P = 0.81).

We did not detect any significant difference between generation scores recorded before and after the experiment (pre- and post-experiment, P = 0.26, on 19 subjects). The mean number of verbs generated over the three

Brain volume

An important finding of this study is the impact of brain volume on functional variability, observed especially in the case of the speech comprehension task. Ideally, when using multiple regression analyses, all relevant predictors (and no irrelevant predictor) of the variable one wants to explain should be included in the model (Grimm and Yarnold, 1995). As a matter of fact, including brain volume improved the multiple regression model not only by its own effect (Josse et al., 2003) but also

Conclusion

Functional imaging offers a parametric assessment of hemispheric specialization for language and its variability, either at the global or regional level, which allowed us to evidence the relevance of brain volume to this complex phenomenon. Previous research on hemispheric specialization for language has evidenced or proposed multiple factors that would influence its variability. These are anatomical, functional, genetic, and physiological factors acting either during the early development of

Subjects

Twenty young French males (22 ± 2.5 years) participated in this study. They were free from neurological disease or cerebral abnormality as assessed on their T1-weighted MRI images. All were selected depending on their ability to generate more than two verbs for one noun in 10 s (Wise et al., 1991). The Edinburgh questionnaire (Oldfield, 1971) was used to assess handedness scores. Eight subjects with scores over zero and who wrote exclusively with the right hand were considered as right-handers,

Acknowledgments

The authors wish to thank Dimitri Papathanassiou, Guy Perchey, and Vincent Beaudouin for the data acquisition as well as Gaël Jobard, Anjali Raja and two anonymous reviewers for the comments on the manuscript. Goulven Josse was supported by a grant from the Commissariat à l'Energie Atomique (CEA) and the Région Basse-Normandie. Pierre-Yves Hervé is supported by a grant from the Ministère de l'Education Nationale et de la Recherche.

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    This work was in part presented at the 10th conference on Human Brain Mapping, Budapest, 2004.

    1

    These authors contributed equally to this work.

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