Visual feedback alters force control and functional activity in the visuomotor network after stroke

Abstract

Modulating visual feedback may be a viable option to improve motor function after stroke, but the neurophysiological basis for this improvement is not clear. Visual gain can be manipulated by increasing or decreasing the spatial amplitude of an error signal. Here, we combined a unilateral visually guided grip force task with functional MRI to understand how changes in the gain of visual feedback alter brain activity in the chronic phase after stroke. Analyses focused on brain activation when force was produced by the most impaired hand of the stroke group as compared to the non-dominant hand of the control group. Our experiment produced three novel results. First, gain-related improvements in force control were associated with an increase in activity in many regions within the visuomotor network in both the stroke and control groups. These regions include the extrastriate visual cortex, inferior parietal lobule, ventral premotor cortex, cerebellum, and supplementary motor area. Second, the stroke group showed gain-related increases in activity in additional regions of lobules VI and VIIb of the ipsilateral cerebellum. Third, relative to the control group, the stroke group showed increased activity in the ipsilateral primary motor cortex, and activity in this region did not vary as a function of visual feedback gain. The visuomotor network, cerebellum, and ipsilateral primary motor cortex have each been targeted in rehabilitation interventions after stroke. Our observations provide new insight into the role these regions play in processing visual gain during a precisely controlled visuomotor task in the chronic phase after stroke.

Keywords: Force control; Ipsilateral M1; Stroke; Visual feedback; Visuomotor network; fMRI.

Fig. 1

Lesion overlap with the sensorimotor area tract template (S-MATT). The S-MATT (A) is comprised of six separate sensorimotor tracts descending from the primary motor cortex (M1), dorsal premotor cortex (PMd), ventral premotor cortex (PMv), supplementary motor area (SMA), pre-supplementary motor area (preSMA), and somatosensory cortex (S1). Each individual's lesion was overlaid on top of each tract within the S-MATT to quantify lesion overlap within the tract (see example in B). The mean lesion overlap for each tract is shown in C, with each column representing the group average. Error bars represent ± SEM.

Fig. 2

Visual gain manipulation. The gain of the visual feedback was altered between functional MRI scans which led to a change in the visual angle of the feedback (A). At larger visual angles, the spatial amplitude of the visual feedback is increased even though the distance in absolute force (N) between the target bar and the force bar remains constant (e.g., 1N) (B). Since visual angle is increased from low to medium to high, there is an increase in the spatial amplitude of the visual feedback (C), which is typically associated with a reduction in force output variability (D).

Fig. 3

Force measures. Mean values for unimpaired/dominant hand force amplitude (A), force error (B), and force variability (C) are shown for control subjects (green) and stroke subjects (red) for all gain levels. Mean values for the impaired/non-dominant hand force amplitude (D), force error (E), and force variability is also shown. Each data point represents the group mean at each level of visual gain, and error bars represent ± SEM.

Fig. 4

Main effect of gain. Results of the main effect of gain obtained from the 3dANOVA in AFNI. Statistical maps were thresholded at P = 0.005 and cluster extent of 216 mm³ for the cortex and 162 mm³ for the cerebellum. The statistic displayed is the F-statistic, with brighter colors indicating more significant voxels which demonstrated changes in BOLD signal with a change in visual gain. Regions with visuomotor importance are marked, with the plots connected to them displaying the average BOLD amplitude at each gain level (yellow data points). Error bars indicate ± SEM, between gain differences are shown in Table 3 (P < 0.05, Bonferroni corrected).

Fig. 5

Main effect of group. Results of the main effect of group obtained from the 3dANOVA in AFNI. Statistical maps were thresholded at P = 0.005 and extent of 216 mm³ for the cortex and 162 mm³ for the cerebellum. The statistic display is the F-statistic, with brighter colors indicating more significant voxels which demonstrated a difference in BOLD signal between groups averaged across gain levels. The average BOLD amplitude for the control group (green) and stroke group (red) is shown. The stroke group displayed increased BOLD amplitude change, compared to controls, at all gain levels (P < 0.05, Bonferroni corrected). Error bars indicate ± SEM. Between group differences across all gain levels are shown in Table 4.

Fig. 6

Gain × group interaction. A conjunction showing the main effect of gain (orange), main effect of group (blue), and group × gain interaction (yellow) is shown. Results of the group x gain interaction were obtained from 3dANOVA in AFNI. Statistical maps were thresholded at P = 0.005 and extent of 216 mm³ for the cortex and 162 mm³ for the cerebellum. Group x gain interaction regions with visuomotor importance are marked, with the plots connected to them displaying the average BOLD amplitude at each gain level for both groups (control: green, stroke: red). Error bars indicate ± SEM. Between-group differences at each gain level are shown in Table 5 (P < 0.05, Bonferroni corrected).