Differential involvement of cortical and cerebellar areas using dominant and nondominant hands: An FMRI study

Abstract

Motor fMRI studies, comparing dominant (DH) and nondominant (NDH) hand activations have reported mixed findings, especially for the extent of ipsilateral (IL) activations and their relationship with task complexity. To date, no study has directly compared DH and NDH activations using an event-related visually guided dynamic power-grip paradigm with parametric (three) forces (GF) in healthy right-handed subjects. We implemented a hierarchical statistical approach aimed to: (i) identify the main effect networks engaged when using either hand; (ii) characterise DH/NDH responses at different GFs; (iii) assess contralateral (CL)/IL-specific and hemisphere-specific activations. Beyond confirming previously reported results, this study demonstrated that increasing GF has an effect on motor response that is contextualised also by the use of DH or NDH. Linear analysis revealed increased activations in sensorimotor areas, with additional increased recruitments of subcortical and cerebellar areas when using the NDH. When looking at CL/IL-specific activations, CL sensorimotor areas and IL cerebellum were activated with both hands. When performing the task with the NDH, several areas were also recruited including the CL cerebellum. Finally, there were hand-side-independent activations of nonmotor-specific areas in the right and left hemispheres, with the right hemisphere being involved more extensively in sensori-motor integration through associative areas while the left hemisphere showing greater activation at higher GF. This study shows that the functional networks subtending DH/NDH power-grip visuomotor functions are qualitatively and quantitatively distinct and this should be taken into consideration when performing fMRI studies, particularly when planning interventions in patients with specific impairments.

Keywords: FMRI; contra-lateral; dominant; force; squeeze-ball.

Figure 1

(A) Illustration of activation maps for DH and NDH on the SUIT flattened cerebellum. Clearly, the anterior and superior posterior ipsilateral cerebellum are involved at each GF. The contralateral cerebellum, on the other hand, is highly involved when using the NDH. (B) Illustration of the involvement of the deep cerebellar nuclei with the task. (a) The dentate cerebellar nuclei (DCN) is the largest nucleus and has a high iron content, therefore appearing hypointense on the EPI template, at either side of the cerebellar midline (green arrow). (b–d) Activations produced by either the DH (top row, red) or NDH (bottom row, blue), at GF levels of b. 20%, c. 40%, d. 60% of maximum voluntary contraction (MVC), (e) Main effect of grip, showing that as the GF increases the DCNs are more engaged, hence indicating an interaction with complexity of both the task and its execution. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Illustration of activations of main effect of movement within the dorsal (PMd) and ventral (PMv) premotor cortex when using either DH or NDH. These maps were generated by masking significant activations (using a threshold of P < 0.001, corrected at the cluster level, for the purpose of illustration) with ROIs localized in the premotor regions using the HMAT template. In the map right is right. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

Illustration of activations of main effect of movement within 15 subregions of the parietal lobe when using DH or NDH. These maps were generated by masking significant activations (using a threshold of P < 0.001, corrected at the cluster level, for the purpose of illustration) with ROIs localized in the parietal regions. In this convention, right is right. Abbreviations are: BA, Brodmann area; L, left; R, right; SPL, superior parietal lobule; IPL, inferior parietal lobule; IPS, anterior intraparietal sulcus; S2, secondary somatosensory cortex. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

One sample t tests at the group level and 60% GF level for (a) DH (red); (b) NDH (blue); (c) fDNH (blue). All clusters are corrected for multiple comparisons after using a threshold of 0.001 (uncorrected) at the voxel level. In the images, right is right and left is left; axial cut at z = 50; coronal cut at y = −54. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 5

One sample t tests at the group level of Linear effect responses using DH (red) and NDH (blue) in (a) precentral gyri; (b) cerebellum IV–V. All clusters are corrected for multiple comparisons after using a threshold of 0.001 (uncorrected) at the voxel level. In the images, right is right and left is left; axial cut at z = 50; coronal cut at y = −54. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 6

Paired t test analyses at the group level and 60% GF level to compare the DH (red) with NDH (blue), or fNDH (blue). (a) Specificity of regions (by comparing DH and NDH); (b) Lateralisation of regions by comparing DH or NDH versus their flipped images; c) Strength of activations by comparing DH and fNDH. All clusters are corrected for multiple comparisons after using a threshold of 0.001 (uncorrected) at the voxel level. In the images, right is right and left is left. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 7

Conjunction analysis—with common areas illustrated in green—at the group level and the 60% GF level of (a) DH (red) and NDH (blue); (b) DH (red) and fNDH (blue). All clusters are corrected for multiple comparisons after using a threshold of 0.001 (uncorrected) at the voxel level. Axial cut at z = 50; coronal cut at y = −54. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 8

The calculated (unstandardized) effect size maps when using the DH (frame A) and NDH (frame B). The effect sizes are reported for each individual analyses at each force level (20, 40, and 60%), the main effect of forces and the linear activations. In the map right is right. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]