Differential Cortical and Subcortical Activations during Different Stages of Muscle Control: A Functional Magnetic Resonance Imaging Study

Abstract

Movement and muscle control are crucial for the survival of all free-living organisms. This study aimed to explore differential patterns of cortical and subcortical activation across different stages of muscle control using functional magnetic resonance imaging (fMRI). An event-related design was employed. In each trial, participants (n = 10) were instructed to gently press a button with their right index finger, hold it naturally for several seconds, and then relax the finger. Neural activation in these temporally separated stages was analyzed using a General Linear Model. Our findings revealed that a widely distributed cortical network, including the supplementary motor area and insula, was implicated not only in the pressing stage, but also in the relaxation stage, while only parts of the network were involved in the steady holding stage. Moreover, supporting the direct/indirect pathway model of the subcortical basal ganglia, their substructures played distinct roles in different stages of muscle control. The caudate nucleus exhibited greater involvement in muscle contraction, whereas the putamen demonstrated a stronger association with muscle relaxation; both structures were implicated in the pressing stage. Furthermore, the subthalamic nucleus was exclusively engaged during the muscle relaxation stage. We conclude that even the control of simple muscle movements involves intricate automatic higher sensory-motor integration at a neural level, particularly when coordinating relative muscle movements, including both muscle contraction and muscle relaxation; the cortical and subcortical regions assume distinct yet coordinated roles across different stages of muscle control.

Keywords: basal ganglia; caudate nucleus; muscle contraction; muscle relaxation; putamen; subthalamus nucleus.

Figure 1

Brain regions activated during different stages of muscle control. (A) Brain activation during the finger pressing stage are displayed on the sagittal and axial planes. (B) Brain activation during the finger holding stage. (C) Brain activation during the relaxation stage. (D) Contrast map of relaxation > pressing. The voxel-wise threshold was set at p < 0.001 and k = 80; p was set at 0.005 for the holding stage. Abbreviations: ACC, anterior cingulate cortex; M1/PMA, primary motor cortex/premotor area; SMA, supplementary motor area; STN, subthalamic nucleus.

Figure 2

Activation in the striatum and mean time course during different stages of muscle control. (A) Brain activation during the finger pressing stage. Significant activation in both the caudate and putamen is shown. There is an obvious peak in the average time course of the caudate corresponding to the pressing stage. (B) Brain activation during the finger holding stage. Significant activation as well as increased BOLD signal are only observed in the caudate. (C) Brain activation during the finger relaxation stage. Significant activation is only observed in the putamen, and not the caudate. Note that there are two obvious peaks in the time course of the putamen corresponding to the pressing and relaxation of the finger, respectively. (D) Superimposed map of the three stages. (E) Contrast map of pressing > relaxation. The voxel-wise threshold was set at p < 0.001 and k = 80 for the finger pressing and relaxation stages, but p < 0.005 for other contrasts. Abbreviations: SMA, supplementary motor area.