Altered sensorimotor cortical oscillations in individuals with multiple sclerosis suggests a faulty internal model

Abstract

Multiple sclerosis (MS) is a demyelinating disease that results in a broad array of symptoms, including impaired motor performance. How such demyelination of fibers affects the inherent neurophysiological activity in motor circuits, however, remains largely unknown. Potentially, the movement errors associated with MS may be due to imperfections in the internal model used to make predictions of the motor output that will meet the task demands. Prior magnetoencephalographic (MEG) and electroencephalographic brain imaging experiments have established that the beta (15-30 Hz) oscillatory activity in the sensorimotor cortices is related to the control of movement. Specifically, it has been suggested that the strength of the post-movement beta rebound may indicate the certainty of the internal model. In this study, we used MEG to evaluate the neural oscillatory activity in the sensorimotor cortices of individuals with MS and healthy individuals during a goal-directed isometric knee force task. Our results showed no difference between the individuals with MS and healthy individuals in the beta activity during the planning and execution stages of movement. However, we did find that individuals with MS exhibited a weaker post-movement beta rebound in the pre/postcentral gyri relative to healthy controls. Additionally, we found that the behavioral performance of individuals with MS was aberrant, and related to the strength of the post-movement beta rebound. These results suggest that the internal model may be faulty in individuals with MS. Hum Brain Mapp 38:4009-4018, 2017. © 2017 Wiley Periodicals, Inc.

Keywords: PMBR; beta frequency; lower extremity; magnetoencephalography.

Figure 1

(A) Depiction of the target matching task. The isometric knee extension force generated by the participant animates the yellow box to ascend vertically to match the green target box. Each trial lasted 5.0 s and was followed by a 5.0 s rest period. If the participant successfully matched the target, the trial ended early and any additional time was added to the 5.0 s of rest. A successful match occurred when the box representing the participant's isometric force was inside the target box for 0.3 s. (B) Depiction of the custom‐built pneumatic force transducer that was positioned just proximal to the lateral malleolus of the participant. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Group averages (mean ± SD) for reaction time, amount of overshoot, average rate of force development to the target, time to initially reach the target, and time to match the target. * p < .05.

Figure 3

Grand averaged time‐frequency plots of the peak sensor, which was located near the leg area of the sensorimotor strip. The same sensor was used in all participants for both the ERD and PMBR analyzes. The analysis was time‐locked to movement onset (top) to assess the beta ERD, and to movement offset (bottom) to assess the PMBR. For the beta ERD analysis (top), movement onset was defined as time 0.0 s and the baseline was defined as −1.6 to −1.2 s. A strong pre‐ and peri‐movement ERD (blue) can be seen from approximately −0.6 to 2.2 s. This response was strongest in the beta range, but also stretched into the alpha range. For the PMBR analysis (bottom), movement offset was defined as time 0.0 s and the baseline was defined as −4.6 to −4.2 s. A strong PMBR (red) could be seen from approximately 1.2 to 4.0 s. As with the ERD, the response was strongest in the beta range, but also stretched down into the alpha band. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

(A) Grand averaged beamformer image of the post‐movement beta rebound (PMBR; 16–26 Hz, 1.9–2.3 s) from all participants indicated that the response was generated by the leg area of the pre/postcentral gyri. (B) Group averaged time series of the beta activity (16–26 Hz) extracted from the peak voxel. Time is shown on the x‐axis, with movement offset occurring at 0.0 s, while relative power (expressed as a percentage from baseline) is shown on the y‐axis. The PMBR was significantly stronger in healthy controls (blue line) relative to patients with MS (orange line) from 1.25 to 1.65 s. The shaded area around each line denotes the standard error of the mean (SEM). [Color figure can be viewed at http://wileyonlinelibrary.com]