Cerebral lateralization of praxis in right- and left-handedness: same pattern, different strength

Abstract

We aimed to investigate the effect of hand effector and handedness on the cerebral lateralization of pantomiming learned movements. Fourteen right-handed and 14 left-handed volunteers performed unimanual and bimanual tool-use pantomimes with their dominant or nondominant hand during fMRI. A left hemispheric lateralization was observed in the right- and left-handed group regardless of which hand(s) performed the task. Asymmetry was most marked in the dorsolateral prefrontal cortex (DLPFC), premotor cortex (PMC), and superior and inferior parietal lobules (SPL and IPL). Unimanual pantomimes did not reveal any significant differences in asymmetric cerebral activation patterns between left- and right-handers. Bimanual pantomimes showed increased left premotor and posterior parietal activation in left- and right-handers. Lateralization indices (LI) of the 10% most active voxels in DLPFC, PMC, SPL, and IPL were calculated for each individual in a contrast that compared all tool versus all control conditions. Left-handers showed a significantly reduced overall LI compared with right-handers. This was mainly due to diminished asymmetry in the IPL and SPL. We conclude that the recollection and pantomiming of learned gestures recruits a similar left lateralized activation pattern in right and left-handed individuals. Handedness only influences the strength (not the side) of the lateralization, with left-handers showing a reduced degree of asymmetry that is most readily observed over the posterior parietal region. Together with similar findings in language and visual processing, these results point to a lesser hemispheric specialization in left-handers that may be considered in the cost/benefit assessment to explain the disproportionate handedness polymorphism in humans.

Figure 1

Some examples of tool and control stimuli. The red line indicates whether the pantomime is bimanual (between objects) or unimanual (under one object). The position of the object determines with which hand the action is performed (or execution dominance in bimanual trials) (left object/left hand, right object/right hand). In bimanual control trials, the side of the vertically aligned egg determines the hand that makes the dominant movement. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 2

Right‐handed group. Whole‐brain activation during (A) unimanual right hand pantomimes and (B) bimanual pantomimes with the right hand leading projected over an inflated cortical surface mesh. C₁: Depicts the contrast between bimanual versus unimanual tool use pantomimes with the right hand (leading). C₂: The same contrast is detailed over the superior part of the brain and overlayed with the activation of a saccadic localizer task (in blue) at alpha (FDR) < 0.001. D: Whole‐brain activation during unimanual left hand pantomimes projected on an inflated cortical mesh. E: Describes the contrast between all tool pantomimes versus all control conditions. Colored boxes are drawn over lateralized regions of activation (red, premotor cortex; blue, dorsolateral prefrontal cortex; green, posterior parietal cortex). All pantomime activation maps at alpha (FDR) < 0.05. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 3

Left‐handed group. Whole‐brain activation during (A) unimanual left hand pantomimes and (B) bimanual pantomimes with the left hand leading projected over an inflated cortical surface mesh. C₁: The contrast between bimanual versus unimanual tool use pantomimes with the left hand (leading). C₂: The same contrast is detailed over the superior part of the brain and overlayed with the activation of a saccadic localizer task (in blue) at alpha (FDR) < 0.001. D: Depicts whole‐brain activation during unimanual right hand pantomimes projected on an inflated cortical mesh. E: Describes the contrast between all tool pantomimes versus all control conditions. Colored boxes are drawn over lateralized regions of activation (red, premotor cortex; blue, dorsolateral prefrontal cortex; green, posterior parietal cortex). All pantomime activation maps at alpha (FDR) < 0.05. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 4

Individual activation patterns and the effect of motor execution. A: Individual activation patterns of right‐ and left‐handed volunteers over the inferior/middle frontal (z = 10) and posterior parietal (z = 50) region. EHI: Edinburgh Handedness Inventory‐score. B: Contrast of the dominant hand tool conditions between right‐ and left‐handers (without control‐correction for motor execution) showing an asymmetric and opposite activation pattern of primary, supplementary, and subcortical motor regions. Activation map at alpha (FDR) < 0.05. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]