Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation

Abstract

The ability to walk independently with the velocity and endurance that permit home and community activities is a highly regarded goal for neurological rehabilitation after stroke. This pilot study explored a functional magnetic resonance imaging (fMRI) activation paradigm for its ability to reflect phases of motor learning over the course of locomotor rehabilitation-mediated functional gains. Ankle dorsiflexion is an important kinematic aspect of the swing and initial stance phase of the gait cycle. The motor control of dorsiflexion depends in part on descending input from primary motor cortex. Thus, an fMRI activation paradigm using voluntary ankle dorsiflexion has face validity for the serial study of walking-related interventions. Healthy control subjects consistently engaged contralateral primary sensorimotor cortex (S1M1), supplementary motor area (SMA), premotor (PM) and cingulate motor (CMA) cortices, and ipsilateral cerebellum. Four adults with chronic hemiparetic stroke evolved practice-induced representational plasticity associated with gains in speed, endurance, motor control, and kinematics for walking. For example, an initial increase in activation within the thoracolumbar muscle representation of S1M1 in these subjects was followed by more focused activity toward the foot representation with additional pulses of training. Contralateral CMA and the secondary sensory area also reflected change with practice and gains. We demonstrate that the supraspinal sensorimotor network for the neural control of walking can be assessed indirectly by ankle dorsiflexion. The ankle paradigm may serve as an ongoing physiological assay of the optimal type, duration, and intensity of rehabilitative gait training.

Figures

Fig. 1

fMRI activations for 12 healthy controls during voluntary and passive ankle dorsiflexion. Left hemisphere on the left in axial view. Arrows at S1M1 on sagittal, coronal, and axial views.

Fig. 2

Homunculus of peak BOLD signal during isolated right-sided movement of the thoracolumbar paraspinal muscles, quadriceps, tibialis anterior, and extensor hallicus in a normal subject. Left hemisphere is on the right of the axial slice.

Fig. 3

Serial single level sagittal and axial (left cerebrum on left) fMRI studies of Subjects (S) 1– 4 in Table 2 as they voluntarily dorsiflex the paretic ankle over the course of making behavioral gains with rehabilitation therapy for walking. Arrows show the representation for the thoracolumbar paraspinal muscles.

Fig. 4

The number of voxels activated (Z > 2.3, P = 0.01) within the manually drawn regions of interest for each subject in Fig. 3 were tabulated and normalized at baseline for follow-up at 2, 4, 6, and 10 weeks of rehabilitation for walking. M1 (contralateral, cl) to the paretic foot (a) and ipsilateral (il) (b) consistently showed a rise, followed by a decline in activated voxels as behavioral gains progressed for the Subjects 2, 3, and 4 with subcortical strokes. A similar rise followed by a decline was evident in cingulate motor area cl (c). Subject 1, who had a frontal infarct, had a pattern of decreasing activation. The responses in supplementary motor areas changed little over time.