Interhemispheric asymmetry of the human motor cortex related to handedness and gender

Abstract

Most people are right-handed, preferring the right hand for skilled as well as unskilled activities, but a notable proportion are mixed-handed, preferring to use the right hand for some actions and the left hand for others. Assuming a structural/functional correlation in the motor system we tested whether asymmetries in hand performance in consistent right and left handers as well as in mixed handers are associated with anatomical asymmetries in the motor cortex. In vivo MR morphometry was used for analyzing interhemispheric asymmetry in the depth of the central sulcus in the region of cortical hand representation of 103 healthy subjects. Subjects were tested both for hand preference and hand performance. As expected, left-right differences in hand performance differed significantly between consistent right, consistent left and mixed handers and were independent on gender. Male consistent right handers showed a significant deeper central sulcus on the left hemisphere than on the right. Anatomical asymmetries decreased significantly from male consistent right over mixed to consistent left handers. Sixty two per cent of consistent left handers revealed a deeper central sulcus on the right than on the left hemisphere, but for the group as a whole this rightward asymmetry was not significant. No interhemispheric asymmetry was found in females. Thus, anatomical asymmetry was associated with handedness only in males, but not in females, suggesting sex differences in the cortical organization of hand movements.

Introduction

Approximately 90% of all subjects are right-handed with men and younger people showing slightly lower frequencies of right-handedness. The remaining 10% of the population are left-handed [22]. Some people belonging to either handedness group do not use one hand exclusively, but favor the right hand for some actions, and the left, for others [46]. Applying the terminology of Annett these subjects can be classified as mixed handers [7]. The prevalence of mixed handers (MH) is estimated to be 33% of the general population whereas the prevalence figures of consistent right (CRH) and consistent left handers (CLH) are approximately 64%, respectively 4% [7]. Right, mixed and left handers as classified applying preference tests can also be distinguished when comparing asymmetry scores of hand performance. The preferred hand clearly dominates in these tests in CRH and CLH whereas both hands show nearly similar performance scores in MH [27].

The neurobiological basis for hand preference and left-right differences in hand performance is still not understood [19], [21]. Although several studies have demonstrated that anatomical asymmetries in the sizes of the frontal and occipital lobes [9], [35], [38], [65], in the surface of the planum temporale and planum parietale [20], [29], [56], [59], [62], [69], [70] and the anterior speech region [3], [17], [18] are correlated with handedness, none of them pinpoints a neurobiological substrate of handedness. Handedness was more or less used as a noninvasive marker of other functional asymmetries (for instance language lateralization).

Surprisingly few theories and studies have focused on anatomical asymmetries directly related to handedness. Older theories dating from the 19th and the beginning of the 20th century proposed that non-neural asymmetries of, e.g., blood supply to the extremities, or of arm length or bone weight were genetically fixed and would determine handedness [25], [26], [61]. A recent study [47] demonstrated that right-handed individuals have larger right than left hands. Based on what is known about trophic interactions between neurons and targets, such findings would seem to predict that the relevant parts of the sensorimotor system are correspondingly asymmetrical. This assumption was partly substantiated by the finding that there is a left-sided asymmetry in the depth of the central sulcus in a sample of post mortem brains with unknown handedness [67].

One of our recent studies measured in vivo the intrasulcal length of the precentral gyrus, i.e., the depth of the central sulcus (CS), as an estimate of the size of the hand motor area. There was a distinct left-larger-than-right asymmetry in right-handed males and a right-larger-than-left asymmetry in left-handed males [2]. In addition, professional right-handed keyboard players who had received intensive bimanual training from early childhood on were more symmetrical both in hand skill tests and in the sulcal depth [1]. These data were obtained in subjects tested for handedness and hand preference and therefore clearly supported the concept that asymmetry in the human motor cortex is linked to an asymmetry in hand performance. In contrast, a recent study demonstrated an interhemispheric symmetry in the depth of the central sulcus in 67 autopsy cases without considering their handedness and gender [66].

The present study was designed in order to analyze the hand motor area by measuring the depth of the central sulcus in horizontal sections of 3-D reconstructed brains in a large sample of healthy young males and females precisely tested for hand preference and hand performance. With these data we evaluated: (1) whether the interhemispheric asymmetry in the size of the hand motor area differs between consistent right, left, and mixed handers; and (2) whether this asymmetry interacts statistically with gender.