Functional somatotopy revealed across multiple cortical regions using a model of complex motor task

Abstract

The primary motor cortex (M1) possesses a functional somatotopic structure-representations of adjacent within-limb joints overlap to facilitate coordination while maintaining discrete centers for individuated movement. We examined whether similar organization exists across other sensorimotor cortices. Twenty-four right-handed healthy subjects underwent functional magnetic resonance imaging (fMRI) while tracking complex targets with flexion/extension at right finger, elbow and ankle separately. Activation related to each joint at false discovery rate of 0.005 served as its representation across multiple regions. Within each region, we identified the center of mass (COM) for each representation, and the overlap between the representations of within-limb (finger and elbow) and between-limb joints (finger and ankle). Somatosensory (S1) and premotor cortices (PMC) demonstrated greater distinction of COM and minimal overlap for within- and between-limb representations. In contrast, M1 and supplementary motor area (SMA) showed more integrative somatotopy with higher sharing for within-limb representations. Superior and inferior parietal lobule (SPL and IPL) possessed both types of structure. Some clusters exhibited extensive overlap of within- and between-limb representations, while others showed discrete COMs for within-limb representations. Our results help to infer hierarchy in motor control. Areas such as S1 may be associated with individuated movements, while M1 may be more integrative for coordinated motion; parietal associative regions may allow switch between both modes of control. Such hierarchy creates redundant opportunities to exploit in stroke rehabilitation. The use of complex rather than traditionally used simple movements was integral to illustrating comprehensive somatotopic structure; complex tasks can potentially help to understand cortical representation of skill and learning-related plasticity.

Keywords: Functional MRI or fMRI; Motor control; Motor map; Movement; Posterior parietal cortex; Primary motor cortex or M1; Representation; Somatotopy.

Figure 1

a and 1b: Experimental description: 1a) Schematic depicting a subject performing a tracking task in the MRI. Task is performed separately at differing joints, right index finger, elbow and ankle, using flexion/extension. Movement at the joint is recorded via special sensors (see section 4.2). Subject uses flexion/extension at the designated joint to follow a moving target waveform presented on a projection screen that is viewed through a rear-projection mirror attached to the MRI head coil. Prompts at the bottom of the screen indicate the block- rest or finger, elbow or ankle tracking. Accuracy of tracking is emphasized as subjects can view their response and its relation to the moving target waveform in real-time. 1b) Repeating sequence of blocks for finger (F), elbow (E), ankle (A) tracking and rest (R).

Figure 2

Cortical Substrates of a tracking: Overall statistical parametric maps of complex visuomotor tracking task tested across upper and lower limb joints (F+E+A vs. rest contrast). Activated regions include supplementary motor area (SMA), premotor cortex (PMC), primary motor cortex (M1), somatosensory cortex (S1), superior parietal lobule (SPL), inferior parietal lobule (IPL), dorsolateral prefrontal cortex (DLPFC) and precuneus (PrCU) in the left and SMA, M1, S1, IPL and DLPFC in the right hemisphere. Regions have only been labeled on the right so that their homologues on the left can be viewed clearly. The color scale represents T-scores of intensity of activation threshold at 4.58, FDR = 0.005.

Figure 3

Activation-based representations of individual joints: Statistical parametric maps (FDR < 0.005) of finger (F), elbow (E) and ankle (A) tracking vs. rest. Activated regions include supplementary motor area (SMA), premotor cortex (PMC), primary motor cortex (M1), somatosensory cortex (S1), superior parietal lobule (SPL) (left hemisphere), inferior parietal lobule (IPL), dorsolateral prefrontal cortex (DLPFC) (right hemisphere) and precuneus (PrCU) (only with finger and ankle tracking in the left hemisphere). The color scale represents T-scores threshold at 4.69 (finger), 4.93 (elbow) and 4.86 (ankle), FDR = 0.005.

Figure 4

Size of Activation: Volume of activation (number of voxels) related to tracking at each joint plotted for each cortical region within the left hemisphere. Tracking at finger elicited the largest volume of activation in M1, S1, PMC, SPL and IPL, where ankle and elbow generated the largest activation in SMA . (*p <.05 and **p <.001).

Figure 5

Overlap: Degree of overlap between finger and elbow (FE) and finger and ankle (FA) in the right and left hemisphere. Values are a percentage of shared voxels within each given region – SMA, PMC, M1, S1, IPL, SPL, PrCU and DLPFC.

Figure 6

Center of Mass: Talairach center of mass between finger (F), elbow (E) and ankle (A) tracking across multiple regions of the brain in the left hemisphere and right hemisphere. Regions represented are primary motor cortex (M1), somatosensory cortex (S1), Premotor Cortex (PMC), supplementary motor area (SMA), inferior parietal lobule (IPL) and superior parietal lobule (SPL). The SPL and IPL demonstrated multiple clusters during F and A activation; they are identified as Fc1, Fc2, Ac1 and Ac2. X, Y, Z-axes coordinates are in mm. All coordinates are represented in table 1 and 2 in bold text. The points represent means (±SD).