Specialization of the left supramarginal gyrus for hand-independent praxis representation is not related to hand dominance

Abstract

Data from focal brain injury and functional neuroimaging studies implicate a distributed network of parieto-fronto-temporal areas in the human left cerebral hemisphere as playing distinct roles in the representation of meaningful actions (praxis). Because these data come primarily from right-handed individuals, the relationship between left cerebral specialization for praxis representation and hand dominance remains unclear. We used functional magnetic resonance imaging (fMRI) to evaluate the hypothesis that strongly left-handed (right hemisphere motor dominant) adults also exhibit this left cerebral specialization. Participants planned familiar actions for subsequent performance with the left or right hand in response to transitive (e.g., "pounding") or intransitive (e.g. "waving") action words. In linguistic control trials, cues denoted non-physical actions (e.g., "believing"). Action planning was associated with significant, exclusively left-lateralized and extensive increases of activity in the supramarginal gyrus (SMg), and more focal modulations in the left caudal middle temporal gyrus (cMTg). This activity was hand- and gesture-independent, i.e., unaffected by the hand involved in subsequent action performance, and the type of gesture (i.e., transitive or intransitive). Compared directly with right-handers, left-handers exhibited greater involvement of the right angular gyrus (ANg) and dorsal premotor cortex (dPMC), which is indicative of a less asymmetric functional architecture for praxis representation. We therefore conclude that the organization of mechanisms involved in planning familiar actions is influenced by one's motor dominance. However, independent of hand dominance, the left SMg and cMTg are specialized for ideomotor transformations-the integration of conceptual knowledge and motor representations into meaningful actions. These findings support the view that higher-order praxis representation and lower-level motor dominance rely on dissociable mechanisms.

Keywords: Apraxia; Dissociable mechanisms; Gesture; Lefthanders; Motor dominance; Parietal cortex; Planning; Praxis; Right-handers; Tool use.

Figure 1. Structure and timing of the fMRI gesture task

The instructional cue (1,500 ms) was followed by a variable delay interval (2,000, 4,000, or 6,000 ms) during which gestures were planned, a movement cue for gesture production (4,000 ms), and a variable inter-trial interval (2,500, 4,500, or 6,500 ms).

Figure 2. Areas activated during gesture planning for the left (panel A) and right (panel B) hand, controlled for linguistic processing

The volumetric surface renderings in the upper panels show significant group effects displayed on the PALs atlas in Caret 5.6 using the multifiducial procedure (see Methods). Clusters that survived multifiducial re-mapping are shown in warm hues. Pale green represents areas that were activated in some individuals (as revealed by the re-mapping algorithm) but did not survive the multifiducial average threshold after accounting for intrasubject variability in gyri and sulci anatomy. Axial slices in the lower panels display significant group mean statistical parametric maps projected onto an average brain obtained from high resolution, T1-weighted anatomical scans of participants’ brains. Neurological convention is used in which right hemisphere is on the right side. The range of the Z statistic values is shown at the bottom and voxels activated at a given Z value are displayed according to the code on the color bar. (A) Praxis planning with the dominant left hand versus the linguistic control (LC) condition. In addition to bilateral signal increases in the dorsal premotor, pre-supplementary motor, cingulate motor area, and rostral middle frontal gyrus (with the latter being substantially more invoked on the left), the inferior parietal lobule was activated only on the left. The left cerebellum and caudal inferior temporal gyrus (cITG) were also involved. (B) Praxis planning with the non-dominant right hand vs. LC. The bilateral activation involved all the major structures typically observed in action planning and/or production, including the right angular, middle frontal, and inferior temporal gyri.

Figure 3. Hand-dependent (panel A) and hand-independent (panel B) neural substrate of praxis planning

(A) When left-handers plan gestures with their right hand, nearly all the areas revealed in an initial contrast of right-hand gesture planning vs. LC are activated more, and more extensively than for the left hand. The inverse contrast (of left vs. right hand) revealed no significant difference. (B) Areas engaged in praxis planning vs. the linguistic control (LC) across both hands. In addition to the dorsal premotor and pre-supplementary motor areas that were activated bilaterally, the left inferior parietal lobule, including the supramarginal gyrus and the ventro-lateral bank of the anterior intraparietal sulcus (SMg/aIPS) was activated only on the left. Additional small cluster of hand-independent activity was observed in cMTg, caudal inferior temporal gyrus (cITg), and the cerebellum on the left.

Figure 4. Region-of-Interest analyses of gesture planning with the dominant left and the non-dominant right hand

The average % signal change during the planning-phase is shown relative to the resting baseline for tool use (transitive) pantomimes and intransitive gestures within the independently defined left SMg (A) and cMTg (B). No significant effects were detected.

Figure 5. Hand-dependent (panel A and B), and hand-independent effects (panel C) during gesture production

(A) A main effect of hand revealing all voxels involved more in the control of the left (vs. right) hand. In addition the expected activity observed in the right hemisphere, including the sensorimotor cortex, posterior parietal, frontal and pre-frontal (MFG) activity, it is worth emphasizing that the left SMg, vPMC and MFg were also involved. (B) A main effect of hand revealing all voxels involved more in the control of the right (vs. left) hand. The activity was primarily limited to the left sensorimotor cortices and a small cluster in the right cerebellum. (C) Areas activated across both hands during gesture production. Except for the right caudal middle temporal cortex (cMTg), all the remaining parieto-frontal, the insular and temporal cortices, as well as subcortical regions were involved bilaterally.

Figure 6. The effect of handedness on gesture planning, and production

(A) Areas involved more in gesture planning in left-handers: Areas engaged more by left-handers were located either in the right hemisphere, i.e. right ANg, dPMC, or bilaterally (dorso-medial, and dorso-lateral prefrontal cortices). (B) Areas involved more in gesture production in left-handers: Again, except for the left-sided early visual and cerebellar contribution, areas engaged more by left-handers were in the dorso-medial prefrontal cortices. (C) Areas involved more in gesture production in right-handers: In addition to left SPL, dPMC, MFg, and some dPMC, and SMg/aIPS, there was also some noticeable involvement of the left anterior STg, and the nearby insular cortex. The right-hemisphere involvement was substantially less pronounced and included some lateral-ventral prefrontal contributions.