Does hand modulate the reshaping of the attentional system during rightward prism adaptation? An fMRI study

Abstract

Adaptation to right-deviating prisms (R-PA), that is, learning to point with the right hand to targets perceived through prisms, has been shown to change spatial topography within the inferior parietal lobule (IPL) by increasing responses to left, central, and right targets on the left hemisphere and decreasing responses to right and central targets on the right hemisphere. As pointed out previously, this corresponds to a switch of the dominance of the ventral attentional network from the right to the left hemisphere. Since the encoding of hand movements in pointing paradigms is side-dependent, the choice of right vs. left hand for pointing during R-PA may influence the visuomotor adaptation process and hence the reshaping of the attentional system. We have tested this hypothesis in normal subjects by comparing activation patterns to visual targets in left, central, and right fields elicited before and after adaptation to rightward-deviating prisms using the right hand (RWRH) with those in two control groups. The first control group underwent adaptation to rightward-deviating prisms using the left hand, whereas the second control group underwent adaptation to leftward-deviating prisms using the right hand. The present study confirmed the previously described enhancement of left and central visual field representation within left IPL following R-PA. It further showed that the use of right vs. left hand during adaptation modulates this enhancement in some but not all parts of the left IPL. Interestingly, in some clusters identified in this study, L-PA with right hand mimics partially the effect of R-PA by enhancing activation elicited by left stimuli in the left IPL and by decreasing activation elicited by right stimuli in the right IPL. Thus, the use of right vs. left hand modulates the R-PA-induced reshaping of the ventral attentional system. Whether the choice of hand during R-PA affects also the reshaping of the dorsal attentional system remains to be determined as well as possible clinical applications of this approach. Depending on the patients' conditions, using the right or the left hand during PA might potentiate the beneficial effects of this intervention.

Keywords: attention; fMRI; functional reshaping; hand; inferior parietal lobule; prism adaptation.

Figure 1

Modulation of brain activation as revealed by the general ANOVA including the three experimental groups (RWRH, RWLH, LWRH). (A) Surface renderings of significant brain activation in the interaction between the factors Group (RWRH, RWLH, LWRH) x Target location (left, center, right) x Session (pre, post), from left to right: lateral views of the left and right hemisphere, view from the back and the top. All maps are thresholded at p < 0.05, cluster extent k > 64. (B) Spheres located on the peaks of activation clusters in the parietal and prefrontal regions. Lateral views of the left and right hemispheres, above the back and top views. Color code denotes names of the regions, as indicated on the y-axis in C. (C) Differences of activation in percent signal change, after minus before PA, for each group (RWRH, RWLH, and LWRH) and each target position (left, center, and right). Asterisks mark two additional regions, which were identified in a previous study by contrasting the effect of R-PA to that of plain glasses (Crottaz-Herbette et al., 2014). Activation thresholded at p = 0,05 and k = 64 (expected numbers of voxels per clusters provided by SPM12) 0.4 AG, angular gyrus; FEF, frontal eye field; IFG, inferior frontal gyrus; L, left; PSC, percent signal change; R, right hemisphere; SFG, superior frontal gyrus; SMG, supramarginal gyrus.

Figure 2

Impact of the hand used during R-PA on the reshaping of visuo-spatial representations. Modulation of brain activation as revealed by the ANOVA including the groups RWRH and RWLH. (A) Surface renderings of significant brain activation in the interaction between the factors Group (RWRH, RWLH) x Target location (left, center, right) x Session (pre, post), from left to right: lateral views of the left and right hemisphere, view from the back and the top. All maps are thresholded at p < 0.05, cluster extent k > 66. (B) Spheres located on the peaks of activation clusters in the parietal and prefrontal regions. Lateral views of the left and right hemispheres, above the back and top views. Color code denotes names of the regions, as indicated on the y-axis in C. (C) Differences of activation in percent signal change, after minus before PA, for each group (RWRH and RWLH) and each target position (left, center, and right). AG, angular gyrus; FEF, frontal eye field; IFG, inferior frontal gyrus; IPL, inferior parietal gyrus; L, left; PSC, percent signal change; R, right hemisphere; SFG, superior frontal gyrus; SMG, supramarginal gyrus; SPL, superior parietal lobule.

Figure 3

Impact of the direction of the prism deviation on the reshaping of visuo-spatial representations. Modulation of brain activation as revealed by the ANOVA including the groups RWRH and LWRH. (A) Surface renderings of significant brain activation in the interaction between the factors Group (RWRH, LWRH) x Session (pre, post), from left to right: lateral views of the left and right hemisphere, view from the back and the top. All maps are thresholded at p < 0.05, cluster extent k > 82. (B) Spheres located on the peaks of activation clusters in the parietal and prefrontal regions. Lateral views of the left and right hemispheres, above the back and top views. Color code denotes names of the regions, as indicated on the x-axis in C. (C) Differences of activation in percent signal change, after minus before PA, for the group RWRH (in red) and LWRH (in green). AG, angular gyrus; FEF, frontal eye field; IFG, inferior frontal gyrus; IPL, inferior parietal gyrus; L, left; PSC, percent signal change; R, right hemisphere; SFG, superior frontal gyrus; SMG, supramarginal gyrus; TPJ, temporo-parietal junction.

Figure 4

Functional heterogeneity of IPL, as revealed by the impact used during R-PA vs. (green dots), the direction of prism deviation (orange dots). The former correspond to peaks of activity determined by three-way ANOVA Group (RWRH, RWLH) x Target location (left, center, right) x Session (pre, post) illustrated in Figure 2, the latter to those of two-way ANOVA Group (RWRH, LWRH) x Session (pre, post) illustrated in Figure 3. Note that in the left hemisphere regions impacted by the hand used during R-PA are located in the supero-medial part of IPL and those impacted by the direction of the prism deviation in the latero-posterior part. Less clear segregation is present in the right hemisphere.