Selective regions of the visuomotor system are related to gain-induced changes in force error

Abstract

When humans perform movements and receive on-line visual feedback about their performance, the spatial qualities of the visual information alter performance. The spatial qualities of visual information can be altered via the manipulation of visual gain and changes in visual gain lead to changes in force error. The current study used functional magnetic resonance imaging during a steady-state precision grip force task to examine how cortical and subcortical brain activity can change with visual gain induced changes in force error. Small increases in visual gain < 1° were associated with a substantial reduction in force error and a small increase in the spatial amplitude of visual feedback. These behavioral effects corresponded with an increase in activation bilaterally in V3 and V5 and in left primary motor cortex and left ventral premotor cortex. Large increases in visual gain > 1° were associated with a small change in force error and a large change in the spatial amplitude of visual feedback. These behavioral effects corresponded with increased activity bilaterally in dorsal and ventral premotor areas and right inferior parietal lobule. Finally, activity in the left and right lobule VI of the cerebellum and left and right putamen did not change with increases in visual gain. Together, these findings demonstrate that the visuomotor system does not respond uniformly to changes in the gain of visual feedback. Instead, specific regions of the visuomotor system selectively change in activity related to large changes in force error and large changes in the spatial amplitude of visual feedback.

Fig. 1.

A: precision grip apparatus held between the thumb and index finger by the subject during the functional magnetic resonance imaging (fMRI) scan. B: si425 Optical Sensing Interrogator (Micron Optics). The force signal was transmitted via fiber-optic wire to the Interrogator outside the fMRI environment. C: visual display viewed by the subject during the Rest and Force with Vision (FV) condition. Participants were instructed to: 1) Rest: fixate on the red target bar, 2) FV: produce isometric force represented by the white bar to match the green target bar that was set at 15% of their maximum voluntary contraction (MVC) with on-line visual feedback. D: exemplar force output (left) and visual feedback (right) data from one subject during the FV condition at each level of visual gain. The dashed green line represents the target force level. Please note that the subject did not view these 2-dimensional time series, but rather a one-dimensional representation as shown in C.

Fig. 2.

Each data point represent the across participant mean at each level of visual gain. Force error (RMSE_N) is represented by filled circles. The spatial amplitude of visual feedback (RMSE_cm) is represented by open circles. Mean force error decreased with an increase in visual gain and post hoc analyses identified the breakpoint at 1°. Mean spatial amplitude of visual feedback increased with an increase in visual gain. Error bars represent ±1SE.

Fig. 3.

Example axial slices showing mean blood oxygenation level dependent (BOLD) activation detected by voxelwise analyses overlaid on a single subject's transformed brain. The color bar ranges from t = 0 to t = 32, with a group activation threshold of P < 0.05, corrected. The corrected t-statistics associated with each voxel are displayed. This figure shows that performing the precision grip force task led to activity in the visuomotor system.

Fig. 4.

A–E: region of interest (ROI) analyses from visuomotor areas that change with a large change in force error. Regression results and post hoc t-test for all visuomotor areas are shown in Table 1. Individual graphs show brain areas that had increased BOLD activation between gain level 1 and gain level 4. Each data point represents the across participant mean at each level of visual gain. Error bars represent ±1SE. L, left, R, right. **P < 0.01; *P < 0.05.

Fig. 5.

A–E: ROI analyses from visuomotor areas that change with a large change in the spatial amplitude of visual feedback. Regression results and post hoc t-test for all visuomotor areas are shown in Table 1. Individual graphs show brain areas that had increased BOLD activation between gain level 4 and gain level 6. Each data point represents the across participant mean at each level of visual gain. Error bars represent ±1SE. L, left; R, right. **P < 0.01; *P < 0.05.