Brain activation associated with active and passive lower limb stepping

Abstract

Reports about standardized and repeatable experimental procedures investigating supraspinal activation in patients with gait disorders are scarce in current neuro-imaging literature. Well-designed and executed tasks are important to gain insight into the effects of gait-rehabilitation on sensorimotor centers of the brain. The present study aims to demonstrate the feasibility of a novel imaging paradigm, combining the magnetic resonance (MR)-compatible stepping robot (MARCOS) with sparse sampling functional magnetic resonance imaging (fMRI) to measure task-related BOLD signal changes and to delineate the supraspinal contribution specific to active and passive stepping. Twenty-four healthy participants underwent fMRI during active and passive, periodic, bilateral, multi-joint, lower limb flexion and extension akin to human gait. Active and passive stepping engaged several cortical and subcortical areas of the sensorimotor network, with higher relative activation of those areas during active movement. Our results indicate that the combination of MARCOS and sparse sampling fMRI is feasible for the detection of lower limb motor related supraspinal activation. Activation of the anterior cingulate and medial frontal areas suggests motor response inhibition during passive movement in healthy participants. Our results are of relevance for understanding the neural mechanisms underlying gait in the healthy.

Keywords: MARCOS; fMRI; locomotion; lower limb; motor control; robot; stepping; supraspinal.

Figure 1

The experimental set-up used in the study. (A) The MR compatible stepper MARCOS was mounted to a 1.5 Tesla Philips Achieva MR-scanner (Reprinted from Hollnagel et al., with permission from Elsevier). (B) Movement onsets were triggered visually by the presentation of the word “MOVE.” A metronome set to 0.5 Hz was presented over the headphones to control movement frequency. Trials of movement were interleaved by an auditory control condition indicated by the word “LISTEN.” A white fixation cross was presented during image acquisition.

Figure 2

Overlay of BOLD-signal during active (green) and passive (red) stepping reveals robust activations in an extended sensorimotor network. Overlapping activations in yellow. The positions of the coronal slices are indicated by the blue lines in the sagittal slice at the bottom. Estimated β-weights and percent signal changes from the ROI-analysis are provided in Table 4. M1/S1, primary sensorimotor cortex; S2, secondary sensory cortex; CMA, cingulate motor area; SMA proper, supplementary motor area proper; L, left hemisphere; R, right hemisphere; P, posterior; A, anterior.

Figure 3

(A) Clusters with higher activation during passive than during active stepping and (B) activation higher during active than during passive stepping. The positions of the axial slices are indicated by the blue lines in the sagittal slice on the right; BG, basal ganglia; LP, lateral parietal cortex; ACC, anterior cingulate cortex; PCC/PC, posterior cingulate cortex/precuneus; SMG, supramarginal gyrus; SMA proper, supplementary motor area proper; L, left hemisphere; R, right hemisphere; P, posterior; A, anterior.