Elsevier

NeuroImage

Volume 54, Issue 2, 15 January 2011, Pages 779-786
NeuroImage

Callosal tracts and patterns of hemispheric dominance: A combined fMRI and DTI study

https://doi.org/10.1016/j.neuroimage.2010.09.072Get rights and content

Abstract

Left-hemispheric dominance for language and right-hemispheric dominance for spatial processing are distinctive characteristics of the human brain. However, variations of these hemispheric asymmetries have been observed, with a minority showing crowding of both functions to the same hemisphere or even a mirror reversal of the typical lateralization pattern. Here, we used diffusion tensor imaging and functional magnetic imaging to investigate the role of the corpus callosum in participants with atypical hemispheric dominance. The corpus callosum was segmented according to the projection site of the underlying fibre tracts. Analyses of the microstructure of the identified callosal segments revealed that atypical hemispheric dominance for language was associated with high anisotropic diffusion through the corpus callosum as a whole. This effect was most evident in participants with crowding of both functions to the right. The enhanced anisotropic diffusion in atypical hemispheric dominance implies that in these individuals the two hemispheres are more heavily interconnected.

Research Highlights

►Atypical hemispheric dominance for language is associated with high anisotropic diffusion in the corpus callosum. ►Typical cerebral asymmetry, such as left-cerebral dominance for language and right-cerebral dominance for spatial processing, is associated with reduced interhemispheric connectivity. ►Crowding of functions to the right hemisphere is associated with especially high anisotropic diffusion in the corpus callosum.

Introduction

The corpus callosum is the largest fibre tract in the human brain connecting the left and right hemispheres and relaying sensory, motor, and higher cognitive information. It is commonly suggested that the corpus callosum plays an important role in the development and maintenance of functional hemispheric asymmetries. The best documented functional asymmetry is the left-hemispheric dominance for language, first described by Paul Broca in the 1860s (Broca, 1861). Non-verbal functions such as spatial attention, face processing, mental rotation, and emotion processing are considered to be right-hemisphere dominant (Bourne, 2008, Corballis, 1997, Vogel et al., 2003).

Handedness is positively correlated with hemispheric dominance for language production, but not with lateralization for spatial processing (Badzakova-Trajkov et al., 2010). The correlation with language dominance has led some to propose a common genetic origin. Genetic models, such as those proposed by Annett, 1998, Annett, 2002 and McManus and Bryden (1992), assume a single gene with one allele predisposing to right-handedness and left-hemispheric dominance for language, and the other leaving the direction of both asymmetries to chance.

Two contrasting models have been suggested for the role of the corpus callosum in brain asymmetry. According to the excitatory model, the corpus callosum integrates information between the hemispheres (Galaburda et al., 1990, Gazzaniga, 2000), so that bilateral processing is associated with enhanced interhemispheric transfer in order to maintain both hemispheres in a functionally activated state. In contrast, the inhibitory model proposes that fibres in the corpus callosum inhibit homotopic areas, allowing for independent functioning of the hemispheres (Cook, 1984). Thus, where the excitatory model predicts a negative correlation between the degree of lateralization and callosal connectivity, the inhibitory model predicts a positive correlation.

Studies based on handedness have been equivocal, with some showing larger callosal areas in left- than in right-handers (Habib et al., 1991, Witelson, 1985, Witelson, 1989, Witelson and Goldsmith, 1991), while others report no differences (Clarke and Zaidel, 1994, Jancke et al., 1997, Preuss et al., 2002, Steinmetz et al., 1992), or even larger callosal areas in right-handers (Westerhausen et al., 2004). Where language lateralization was measured more directly, for example with the dichotic-listening task, correlations between the degree of lateralization and the midsagittal area of the corpus callosum have been negative (Gootjes et al., 2006, Hines et al., 1992, Yazgan et al., 1995), favouring the excitatory model. Similarly, bilateral processing of spatial stimuli, as indicated by a smaller leftward bias in the line-bisection test, was associated with larger callosal areas (Yazgan et al., 1995).

Using fMRI during word generation to measure language lateralization and diffusion tensor imaging (DTI) to examine the microstructure of the corpus callosum, Westerhausen et al. (2006) found that molecular diffusion (MD) in the corpus callosum was lower, while fractional anisotropy (FA) tended to be higher, in strongly left-lateralized subjects than in moderately left-lateralized, bilateral, or right-lateralized subjects, but the groups did not differ with respect to the area of the corpus callosum. The authors interpreted the MD and FA results as indicating stronger and/or faster interhemispheric connections in the strongly left-lateralized individuals, which might be taken as support for the inhibitory model. Josse et al. (2008) found that increased callosal size was associated with greater left-hemisphere activity during language tasks in posterior temporal and inferior frontal regions, together with reduced right-hemisphere activity in posterior temporal regions, again supporting an inhibitory model. In this study, though, participants with right-hemispheric language dominance were excluded.

From an evolutionary perspective, Gazzaniga (2000) has proposed that callosal function was reduced in humans relative to that in primates, to allow differential specialization of the hemispheres. Nevertheless, sufficient interhemispheric connections were retained to permit computations in the two hemispheres to be integrated. On this view, one would predict reduced callosal function in people with the typical pattern of cerebral asymmetry, including left-hemisphere dominance for language and right-hemisphere dominance for spatial processing, compared to those with atypical cerebral asymmetry, especially where the same hemisphere is dominant for both language and spatial processing. Here, we aimed to test this prediction using fMRI to assess lateralization for language and spatial processing, and fractional anisotropy (FA) to measure the efficacy of callosal projections. Increased FA can be found in white matter with more tightly packed axons, thicker myelin sheath, fewer obliquely oriented fibres, and different radii of individual axons (Chepuri et al., 2002). Our main hypothesis was that FA should be higher in those with atypical patterns of cerebral asymmetry.

Section snippets

Subjects

A total of 60 participants took part in the study (30 males with a mean age of 20.83, SD 4.6 and 30 females with a mean age of 23.23, SD 4.55). To establish handedness, all participants filled out a handedness questionnaire (Annett, 2002), consisting of 12 different questions on hand preference (writing, throwing a ball, holding a racquet, lighting a match, cutting with scissors, threading through a needle, broom sweeping, shovelling, dealing cards, hammering, holding a toothbrush, and

fMRI results

All participants completed the Word Generation Task, but one participant did not complete the Landmark Task. The results are graphically displayed in Fig. 1 and the significantly activated brain areas are summarized in Table 1. For the Word Generation Task, significant activations were found in the precentral gyrus, inferior frontal gyrus, insula, SMA and middle occipital gyrus predominantly in the left hemisphere. The activation maps for the Landmark Task showed significant clusters in middle

Discussion

Based on the Word Generation Task, 24% of the left-handers were considered to have atypical language lateralization, which fits well with earlier reports of between 22% (Szaflarski et al., 2002) and 24% (Pujol et al., 1999) of left-handers found to be bilateral or right-hemispheric dominant for language. The incidence of 8% of atypical lateralization for right-handers is slightly higher than in older studies with the Wada test, where estimates range around 4% (Rasmussen and Milner, 1977).

Acknowledgment

This work was supported by a grant to MCC from the Marsden Fund (UOA-0710) administered by The Royal Society of New Zealand.

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