Locomotor patterns during obstacle avoidance in children with cerebral palsy

Abstract

We investigated how early injuries to developing brain affect the interaction of locomotor patterns with the voluntary action required by obstacle clearance. This task requires higher cognitive load and specific anticipatory sensorimotor integration than more automated steady-state gait. To this end, we compared the adaptive gait patterns during obstacle clearance in 40 children with cerebral palsy (CP) (24 diplegic, 16 hemiplegic, 2-12 years) and 22 typically developing (TD) children (2-12 years) by analyzing gait kinematics, joint moments during foot elevation, EMG activity of 11 pairs of bilateral muscles and muscle modules evaluated by factorization of the EMG signals. The results confirmed generally slower task performance, plus difficulty in motor planning and control in CP. Thus, about 30% of diplegic children failed to perform the task. Children with CP demonstrated higher foot lift, smaller range of motion of distal segments, difficulties in properly activating the hamstring muscles at lift-off and a modified hip strategy when elevating the trailing limb. Basic muscle modules were generally roughly similar to TD patterns, though they showed a limited adaptation. Thus, a distinct activation burst in the adaptable muscle module timed to the voluntary task (lift-off) was less evident in CP. Children with CP also showed prolonged EMG burst durations. Impaired obstacle task performance may reflect impaired or less adaptable supraspinal and spinal control of gait when a locomotor task is superimposed with the voluntary movement. Neurorehabilitation of gait in CP may thus be beneficial by adding voluntary tasks such as obstacle clearance during gait performance.

Maturation of the Locomotor Circuitry in Children With Cerebral Palsy

“…In general, children with CP have difficulties in clearing an obstacle, being slower in approach and crossing speed along with unsteadiness of gait and balance adaptations of the trunk control (Law and Webb, 2005;Malone et al, 2016). For instance, in a recent study (Cappellini et al, 2020) we showed that about 30% of children with bilateral CP failed to perform the task (they stopped before the obstacle, performed lateral obstacle avoidance, stumbled or stepped onto the obstacle). Interestingly, they had mostly posterior lesions of the brain (Cappellini et al, 2020), in relation to their deficits in the anticipatory visuomotor control and important role of parietal lobe activity in visually planning gait adaptations (Drew et al, 2008;Lajoie et al, 2010;Drew and Marigold, 2015).…”

“…For instance, in a recent study (Cappellini et al, 2020) we showed that about 30% of children with bilateral CP failed to perform the task (they stopped before the obstacle, performed lateral obstacle avoidance, stumbled or stepped onto the obstacle). Interestingly, they had mostly posterior lesions of the brain (Cappellini et al, 2020), in relation to their deficits in the anticipatory visuomotor control and important role of parietal lobe activity in visually planning gait adaptations (Drew et al, 2008;Lajoie et al, 2010;Drew and Marigold, 2015). Remaining children with CP (∼70%), who succeeded with obstacle clearance, performed the task significantly slower than age-matched TD children, demonstrating a high foot lift of the trailing (unseen) limb, smaller range of motion and muscle moments of the distal (ankle) joint ( Figure 5A, left panels), and limited adaptation of task-relevant activity of hamstring muscles timed to the voluntary task of foot lift over the obstacle (Cappellini et al, 2020).…”

“…Interestingly, they had mostly posterior lesions of the brain (Cappellini et al, 2020), in relation to their deficits in the anticipatory visuomotor control and important role of parietal lobe activity in visually planning gait adaptations (Drew et al, 2008;Lajoie et al, 2010;Drew and Marigold, 2015). Remaining children with CP (∼70%), who succeeded with obstacle clearance, performed the task significantly slower than age-matched TD children, demonstrating a high foot lift of the trailing (unseen) limb, smaller range of motion and muscle moments of the distal (ankle) joint ( Figure 5A, left panels), and limited adaptation of task-relevant activity of hamstring muscles timed to the voluntary task of foot lift over the obstacle (Cappellini et al, 2020). Thus, impaired task performance in children with CP may reflect basic developmental deficits in the adaptable control of gait when the locomotor task is superimposed with the voluntary movement, suggesting that gait rehabilitation strategies should involve tasks performed in challenging environments to enhance the functional capacity of gait controllers.…”

“…To sum up, early injuries to developing brain affect both normal walking and other forms of locomotor behavior: complex locomotor movements (Law and Webb, 2005;Dixon et al, 2016;Mawase et al, 2016;Lewerenz et al, 2019;Cappellini et al, 2020), running (Böhm and Döderlein, 2012), weighting of legs (Bulea et al, 2017), backward walking (Cappellini et al, 2018), and even FIGURE 5 | Adaptive locomotion in children with CP. (A) Obstacle task performance in children with bilateral CP.…”

“…Asterisks denote significant side differences. Adapted from Cappellini et al (2020). (B) Kinematics of forward and backward walking in TD and children with bilateral CP.…”