Feedforward neural control of toe walking in humans

Abstract

Toe walking requires careful control of the ankle muscles in order to absorb the impact of ground contact and maintain a stable position of the joint. The present study aimed to clarify the peripheral and central neural mechanisms involved. Fifteen healthy adults walked on a treadmill (3.0 km h ). Tibialis anterior (TA) and soleus (Sol) EMG, knee and ankle joint angles, and gastrocnemius-soleus muscle fascicle lengths were recorded. Peripheral and central contributions to the EMG activity were assessed by afferent blockade, H-reflex testing, transcranial magnetic brain stimulation (TMS) and sudden unloading of the planter flexor muscle-tendon complex. Sol EMG activity started prior to ground contact and remained high throughout stance. TA EMG activity, which is normally seen around ground contact during heel strike walking, was absent. Although stretch of the Achilles tendon-muscle complex was observed after ground contact, this was not associated with lengthening of the ankle plantar flexor muscle fascicles. Sol EMG around ground contact was not affected by ischaemic blockade of large-diameter sensory afferents, or the sudden removal of ground support shortly after toe contact. Soleus motor-evoked potentials elicited by TMS were facilitated immediately after ground contact, whereas Sol H-reflexes were not. These findings indicate that at the crucial time of ankle stabilization following ground contact, toe walking is governed by centrally mediated motor drive rather than sensory driven reflex mechanisms. These findings have implications for our understanding of the control of human gait during voluntary toe walking.

Maturation of feedforward toe walking motor program is impaired in children with cerebral palsy

“…The adult participants (Fig. 1A, red) shows the characteristic features of controlled toe walking, which have already been reported in adults (Lorentzen et al 2018): 1) Initiation of Sol EMG activity 50-100 ms prior to ground contact, 2) a quick dorsiflexion movement of the ankle joint at ground contact, 3) pronounced Sol EMG activity in early stance with a clear burst of EMG activity 50-100 ms after ground contact and 4) absence of TA EMG activity during the stance phase. The first three features may also be observed in the TD child voluntarily toe walking (Fig.…”

“…In adults, toe walking is controlled by a feedforward motor program, which involves prediction of the mechanical consequences of ground impact and ensures constant step-to-step control of the ankle joint position (Lorentzen al. 2018).…”

“…Drop of the heel following ground contact was calculated as the difference in ankle joint position at ground contact and the most dorsiflexed ankle joint position within the initial 150 ms after ground contact (cf. Lorentzen et al 2018).…”

“…Recent theories in computational motor neuroscience postulate that movements are generated in a feedforward manner, where sensory feedback is predicted more or less precisely (Shadmehr et al 2010, Wolpert et al 2011, Wolpert & Flanagan 2016 and with repetition the movement is optimized through a reduction in the difference between the predicted and actual sensory feedback (Wolpert & Flanagan 2016). It has been recently demonstrated that when adults walk on their toes they use a feedforward motor program, which involves activation of plantar flexor muscles 50-100 ms prior to ground contact (Lorentzen et al 2018). Lorentzen et al (2018) found that the muscle activity around ground contact was unchanged when sensory feedback from the ankle was blocked by ischemia or when the ground was suddenly removed as evidence of the feedforward nature of the muscle activity.…”

“…It has been recently demonstrated that when adults walk on their toes they use a feedforward motor program, which involves activation of plantar flexor muscles 50-100 ms prior to ground contact (Lorentzen et al 2018). Lorentzen et al (2018) found that the muscle activity around ground contact was unchanged when sensory feedback from the ankle was blocked by ischemia or when the ground was suddenly removed as evidence of the feedforward nature of the muscle activity. It is likely that this feedforward motor program requires several years of practice during childhood to be as efficient and precise as in adults.…”