Shoulder apprehension impacts large-scale functional brain networks

Abstract

Backround and purpose: Shoulder apprehension is defined as anxiety and resistance in patients with a history of anterior glenohumeral instability. It remains unclear whether shoulder apprehension is the result of true recurrent instability or a memorized subjective sensation. We tested whether visual presentation of apprehension videos modifies functional brain networks associated with motor resistance and anxiety.

Materials and methods: This prospective study includes 15 consecutive right-handed male patients with shoulder apprehension (9 with right shoulder apprehension, 6 with left shoulder apprehension; 27.5 ± 6.4 years) and 10 healthy male right-handed age-matched control participants (29.0 ± 4.7 years). Multimodal MR imaging included 1) functional connectivity tensorial independent component analysis, 2) task-related general linear model analysis during visual stimulation of movies showing typical apprehension movements vs control videos, 3) voxel-based morphometry analysis of GM, and 4) tract-based spatial statistics analysis of WM.

Results: Patients with shoulder apprehension had significant (P < .05 corrected) increase in task-correlated functional connectivity, notably in the bilateral primary sensory-motor area and dorsolateral prefrontal cortex and, to a lesser degree, the bilateral dorsomedial prefrontal cortex, anterior insula, and dorsal anterior cingulate cortex (+148% right, +144% left). Anticorrelated functional connectivity decreased in the higher-level visual and parietal areas (-185%). There were no potentially confounding structural changes in GM or WM.

Conclusions: Shoulder apprehension induces specific reorganization in apprehension-related functional connectivity of the primary sensory-motor areas (motor resistance), dorsolateral prefrontal cortex (cognitive control of motor behavior), and the dorsal anterior cingulate cortex/dorsomedial prefrontal cortex and anterior insula (anxiety and emotional regulation).

Fig 1.

Visual rating ranging from unpleasant (−1) to pleasant (+1) associated with the presentation of APPREHENSION and CONTROL videos for patients and healthy volunteers. APPREHENSION vs CONTROL videos were associated with reduced rating values for both groups (P < .0001 corrected patients; P < .001 corrected control volunteers). APPREHENSION videos were associated with lower rating scores when comparing patients vs healthy volunteers (P < .01 corrected), whereas there was no significant effect for CONTROL videos.

Fig 2.

Patients vs control participants had a significantly (P < .05 corrected) higher task-correlated functional connectivity in 2 almost mirror symmetric components (IC 12 + 148% Smode in the right hemisphere; IC 17 + 144% Smode in left hemisphere). These networks include the primary sensory-motor areas compatible with motor resistance, dlPFC associated with cognitive control of motor behavior and dACC/dmPFC associated with emotional regulation. In contrast, patients had significantly reduced functional connectivity in a bilateral higher-level visual and parietal network (IC 30 −185% Smode). Moreover, this component is anticorrelated with the video presentation, in contrast to the components IC 12 and IC 17. Axial sections of the spatial representation of the ICs 12, 17, and 30 are illustrated at the top. The inserts at the bottom represent the average time courses of these ICs (left) and the corresponding Fourier spectra (right).

Fig 3.

Correlation analysis between the Smodes (measure of activation strength) of task-positive (ICs 12 and 17) minus task-negative (IC 30) networks, and the participant average behavioral rating of unpleasantness. The negative correlation (rho = −0.4687) was significant (P = .022). Red “x” indicates individual patients; blue “o” indicates individual healthy volunteer data.

Fig 4.

Hypothesis-driven GLM analysis for contrast of APPREHENSION videos vs CONTROL videos. Patients vs healthy volunteers had increased activation in the left primary sensory-motor area and dlPFC overlapping with IC 17, yet at a lower degree of significance. The corresponding contralateral regions showed a clear trend, which remained just below multiple comparisons corrected threshold (not shown). The inverse comparison of healthy volunteers vs patients yielded no significant differences.