Weak but Critical Links between Primary Somatosensory Centers and Motor Cortex during Movement

Abstract

Motor performance is improved by stimulation of the agonist muscle during movement. However, related brain mechanisms remain unknown. In this work, we perform a functional magnetic resonance imaging (fMRI) study in 21 healthy subjects under three different conditions: (1) movement of right ankle alone; (2) movement and simultaneous stimulation of the agonist muscle; or (3) movement and simultaneous stimulation of a control area. We constructed weighted brain networks for each condition by using functional connectivity. Network features were analyzed using graph theoretical approaches. We found that: (1) the second condition evokes the strongest and most widespread brain activations (5147 vs. 4419 and 2320 activated voxels); and (2) this condition also induces a unique network layout and changes hubs and the modular structure of the brain motor network by activating the most "silent" links between primary somatosensory centers and the motor cortex, particularly weak links from the thalamus to the left primary motor cortex (M1). Significant statistical differences were found when the strength values of the right cerebellum (P < 0.001) or the left thalamus (P = 0.006) were compared among the three conditions. Over the years, studies reported a small number of projections from the thalamus to the motor cortex. This is the first work to present functions of these pathways. These findings reveal mechanisms for enhancing motor function with somatosensory stimulation, and suggest that network function cannot be thoroughly understood when weak ties are disregarded.

Keywords: functional connectivity; functional magnetic resonance imaging; graph theory; motor control; weighted brain network.

Figure 1

Brain activations. Activations evoked by different conditions are projected onto the normalized 3D brain with the BrainNet Viewer (http://www.nitrc.org/projects/bnv/). The threshold was set at a family-wise error rate correction of P < 0.05 with a minimum cluster extent of 10 contiguous voxels. The bottom row shows commonly activated areas shared by all three conditions; the last column is the midsagittal view of the left hemisphere. The colored bar indicates t values. Task+AgonistStim evokes the most extensive brain activations. Top to bottom rows consist of 2370, 5147, 4419 and 2320 activated voxels, respectively.

Figure 2

Node degree/strength values. (A) Degree values. The degree of a node is the number of links connected to this node. The thalamus, right cerebellum and left cerebellum exhibit the lowest degree values in all networks (only exception is the left putamen in the Task+AgonistStim network). R, right; L, left; SMA, supplementary motor area; M1, primary motor cortex; CMA, cingulate motor area; PMd, dorsal premotor cortex; PMv, ventral premotor cortex; MFG, middle frontal gyrus; S1, primary somatosensory area; SPL, superior parietal lobule; IPC, inferior parietal cortex; S2, secondary somatosensory area. (B) Strength values. Node strength is the sum of weights of all links connected to this node. The thalamus, right cerebellum and left cerebellum show the lowest strength values in all networks (except for L_Putamen in the Task+AgonistStim network). Error bars show ±SD. (C) Percentage changes in strength values. We use the strength value of each node in the Task network as the baseline (100%). The thalamus, right cerebellum and left cerebellum are nodes with overt increases in strength values in the Task+AgonistStim network, especially the right cerebellum. The Task+ControlStim network shows a distinctive pattern.

Figure 3

Different layouts of networks. Layouts are generated using the Kamada–Kawai force-spring layout algorithm (http://pajek.imfm.si). Nodes/links are sized according to their strength values or connection weights. This visualization method shows how brain regions are organized in a network. Each network shows a large “core” composed of densely-linked nodes with some sparsely connected peripheral nodes.

Figure 4

Betweenness values of nodes. (A) Many nodes have zero values and are superpositioned on the x axis. Topmost nodes in the Task network are L_SMA and L_M1, indicating that these nodes are network hubs. The changes of the two nodes show opposite trends in the Task+AgonistStim network when compared with the Task network, i.e., a higher L_SMA and a lower L_M1 values. Thus, stimulating the agonist muscle remarkably changes the hub of the original network. (B) Results of the post hoc profile analysis. Blue circles indicate nodes with increased betweenness values in the Task+AgonistStim network when compared with the Task network (Nodes 1). Green circles represent nodes with decreased or unchanged values (Nodes 2). Two groups of nodes demonstrate different trends among three conditions (i.e., unparalleled profiles).

Figure 5

Modules of each network in anatomical space. (A) Three networks are visualized with the BrainNet Viewer in the coronal view. Nodes are sized according to nodal strength, and links are sized according to the weight. Nodes in the same module are indicated by the same color. The Task+ControlStim network shows a similar modular structure with the Task network, whereas the Task+AgonistStim network exhibits unique modularity. (B) Links among nodes of the new module (blue nodes in the Task+AgonistStim network). Increased numbers of links are observed in three nodes L_thalamus, L_cerebellum and R_cerebellum, especially the thalamus, under conditions receiving sensory stimulation. (C) Links between two major centers for cortical motor outputs (L_SMA and L_M1) and three primary sensory relay stations. Only the Task+AgonistStim network shows the link between L_M1 and three primary somatosensory centers (L_Thalamus-L_M1).