Contribution of sensory feedback to plantar flexor muscle activation during push-off in adults with cerebral palsy

Abstract

Exaggerated sensory activity has been assumed to contribute to functional impairment following lesion of the central motor pathway. However, recent studies have suggested that sensory contribution to muscle activity during gait is reduced in stroke patients and children with cerebral palsy (CP). We investigated whether this also occurs in CP adults and whether daily treadmill training is accompanied by alterations in sensory contribution to muscle activity. Seventeen adults with CP and 12 uninjured individuals participated. The participants walked on a treadmill while a robotized ankle-foot orthosis applied unload perturbations at the ankle, thereby removing sensory feedback naturally activated during push-off. Reduction of electromyographic (EMG) activity in the soleus muscle caused by unloads was compared and related to kinematics and ankle joint stiffness measurements. Similar measures were obtained after 6 wk of gait training. We found that sensory contribution to soleus EMG activation was reduced in CP adults compared with uninjured adults. The lowest contribution of sensory feedback was found in participants with lowest maximal gait speed. This was related to increased ankle plantar flexor stiffness. Six weeks of gait training did not alter the contribution of sensory feedback. We conclude that exaggerated sensory activity is unlikely to contribute to impaired gait in CP adults, because sensory contribution to muscle activity during gait was reduced compared with in uninjured individuals. Increased passive stiffness around the ankle joint is likely to diminish sensory feedback during gait so that a larger part of plantar flexor muscle activity must be generated by descending motor commands.NEW & NOTEWORTHY Findings suggest that adults with cerebral palsy have less contribution of sensory feedback to ongoing soleus muscle activation during push-off than uninjured individuals. Increased passive stiffness around the ankle joint is likely to diminish sensory feedback during gait, and/or sensory feedback is less integrated with central motor commands in the activation of spinal motor neurons. Consequently, muscle activation must to a larger extent rely on descending drive, which is already decreased because of the cerebral lesion.

Keywords: cerebral palsy; gait; muscle activation; push-off; sensory feedback.

Fig. 1.

A: experimental setup for evaluating the contribution of sensory feedback to plantar flexor muscle activation. Participants walked on a treadmill while wearing a custom-designed electrohydraulic ankle-foot orthosis (EHO). In late stance phase, mechanical power from the electric motor was transferred by hydraulic actuators to the EHO, causing rapid plantar flexor perturbations to the ankle joint, which unloaded the plantar flexor muscles during push-off. B–G: examples of average recorded data during control steps (solid lines) and steps with unload perturbations (dashed lines) of the plantar flexors. Perturbation time is indicated by vertical dotted lines. Data in B–D represent an uninjured participant; data in E–G represent a participant with CP. B and E: soleus muscle EMG; shaded area represents the area under the curve used to calculate the reduction in soleus EMG activity caused by unloading the plantar flexors (unload response). C and F: torque deviation produced by the ankle-foot orthosis used to unload the plantar flexors. D and G: ankle position; dashed line shows the amplitude of the ankle deviation toward planter flexion used to unload the plantar flexors.

Fig. 2.

Average group differences between participants with CP and uninjured participants with individual data point for each group. Values are onset latency (A), duration (B), and size (C) of the reduction in soleus EMG activity following unloading the plantar flexors during late stance phase of gait. Error bars indicate the SD. *P < 0.05 indicates statistical significance.

Fig. 3.

Relationship between the size of the reduction in soleus EMG activity following unloading ankle plantar flexors and maximal gait speed during treadmill walking (A) and overground walking (B) in participants with CP.

Fig. 4.

Relationship between the size of reduction in soleus EMG activity following unloading of ankle plantar flexors and passive stiffness (A), reflex-mediated stiffness (B) and Modified Ashworth Scale (MAS) score (C) in participants with CP.

Fig. 5.

Reduction in soleus EMG activity following unloading of the plantar flexors before (filled bars) and after (open bars) 30 min of daily uphill treadmill gait training for 6 wk in the training group (n = 8) and the control group (n = 9). Error bars indicate SD.