Chronic musculoskeletal impairment is associated with alterations in brain regions responsible for the production and perception of movement

Abstract

Key points: Massive irreparable rotator cuff tear was used as a model to study the impact of chronic pain and motor impairment on the motor systems of the human brain using magnetic resonance imaging. Patients show markers of lower grey/white matter integrity and lower functional connectivity compared with control participants in regions responsible for movement and the perception of visual movement and body shape. An independent cohort of patients showed relative deficits in the perception of visual motion and hand laterality compared with an age-matched control group. These data support the hypothesis that the structure and function of the motor control system differs in patients who have experienced chronic motor impairment. This work also raises a new hypothesis, supported by neuroimaging and behaviour, that a loss of motor function could also be associated with off-target effects, namely a reduced ability to perceive motion and body form.

Abstract: Changes in the way we move can induce changes in the brain, yet we know little of such plasticity in relation to musculoskeletal diseases. Here we use massive irreparable rotator cuff tear as a model to study the impact of chronic motor impairment and pain on the human brain. Cuff tear destabilises the shoulder, impairing upper-limb function in overhead and load-bearing tasks. We used neuroimaging and behavioural testing to investigate how brain structure and function differed in cuff tear patients and controls (imaging: 21 patients, age 76.3 ± 7.68; 18 controls, age 74.9 ± 6.59; behaviour: 13 patients, age 75.5 ± 10.2; 11 controls, age 73.4 ± 5.01). We observed lower grey matter density and cortical thickness in cuff tear patients in the postcentral gyrus, inferior parietal lobule, temporal-parietal junction and the pulvinar - areas implicated in somatosensation, reach/grasp and body form perception. In patients we also observed lower functional connectivity between the motor network and the middle temporal visual cortex (MT), a region involved in visual motion perception. Lower white matter integrity was observed in patients in the inferior fronto-occipital/longitudinal fasciculi. We investigated the cognitive domains associated with the brain regions identified. Patients exhibited relative impairment in visual body judgements and the perception of biological/global motion. These data support our initial hypothesis that cuff tear is associated with differences in the brain's motor control regions in comparison with unaffected individuals. Moreover, our combination of neuroimaging and behavioural data raises a new hypothesis that chronic motor impairment is associated with an altered perception of visual motion and body form.

Keywords: brain; cortex; motor; plasticity; rotator cuff.

Figure 1. Patients with massive irreparable rotator cuff tear show reduced shoulder function (A, lower OSS) and higher levels of pain intensity (B, BPI‐sf) than unaffected control participants

Data shown for Study A cohort; equivalent values for Study B are reported in the main text. Median indicated by bold lines; quartiles indicated by dashed lines. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 2. Evidence of localised cortical regions of lower cortical grey matter density and cortical thickness in cuff tear patients

A and B, massive irreparable rotator cuff tear patients have lower grey matter density in left primary somatosensory cortex, left inferior parietal lobule, right temporal–parietal junction, and left thalamus (posterior parietal projection) (P _FWE < 0.05, TFCE). See Table 1 for all cluster locations. C and D, cuff tear patients also show lower cortical thickness in right temporal–parietal junction, right superior temporal sulcus, and right inferior temporal cortex (vertex‐wise threshold P < 0.001; cluster‐wise threshold P < 0.05). E, neurosynth keyword meta‐analysis shows cognitive functions and brain areas co‐localised to brain regions identified in A from 14,300 reference fMRI studies; word size ≈ strength of association with the spatial map scaled by Z‐score (max: 8.9; min: 3.6). [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3. Massive irreparable rotator cuff tear patients show reduced functional connectivity between the motor network and MT cortex, which is implicated in motion and action perception

A, group mean resting‐state motor network. B, group comparison of the strength of motor network connectivity reveals no global difference between groups. C, a dual regression analysis identified a region of MT as a region of differing functional connectivity with the resting‐state motor network between cuff tear patients and control participants. D, post hoc visualisation of the functional connectivity measures in the region of MT identified. E, keyword meta‐analysis using Neurosynth to quantify the strength of associations between specific cognitive functions and the brain regions identified in C from ∼14,300 reference fMRI studies. Word size represents relative strength of association with spatial map (Z‐score: max, 9.88; min, 3.48). RSN, resting‐state network. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 4. TBSS reveal evidence of reduced white matter integrity in localised regions including right inferior frontal occipital fasciculus and inferior longitudinal fasciculus

A, cuff tear patients showed lower FA in localised white matter regions including right inferior frontal‐occipital fasciculus, inferior longitudinal fasciculus and optic radiations, including areas directly adjacent to grey matter and functional connectivity differences (Figs 2 and 3). B, post hoc visualisation of FA values in significant regions across groups. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 5. Summary of multimodal structural and functional differences between cuff tear patients and controls co‐localised to a cortical region associated with motion and action observation

Observed differences in grey matter density (red), white matter integrity (blue) and functional connectivity of the motor network (orange), derived from three entirely independent modalities and analyses, are co‐localised to a region responsible for body perception and motion. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 6. Massive irreparable rotator cuff tear patients exhibit poorer performance in tasks of body and motion perception compared with unaffected control participants

A cohort independent of the brain imaging data set show evidence of diminished perceptual abilities in tasks associated with the cortical regions identified from the brain imaging data presented in Figs 2–4. Cuff tear patients were significantly slower in their judgement of hand laterality in a body perception task (A). Cuff tear patients also showed significantly higher perceptual thresholds (i.e. poorer performance) in tasks of visual global motion perception (B) and visual biological motion perception (C) compared with unaffected controls. Cuff tear patients did not differ from the control group in low level visual perception of contrast or acuity. [Color figure can be viewed at wileyonlinelibrary.com]