Motor programmes for the termination of gait in humans: organisation and velocity-dependent adaptation

The organisation of the muscular activities responsible for the termination of gait, their modulation as a function of the rate of progression and the associated mechanical effects were investigated in normal adults, using EMG, force plate and kinematic recordings. In particular, the braking actions in reaction to a visual cue presented at the instant of heel-strike were analysed quantitatively, with a focus on representative leg and thigh muscles of the weight-supporting (stance) and oscillating (swing) limb, during walk-and-stop trials performed at three different velocities. In the stance limb, the EMG associated with braking started approximately 150 ms after the stop signal and, on average, displayed a distal-to-proximal activation sequence that primarily involved the posterior muscle groups (soleus, SOL, and hamstring, HAM). With the exception of SOL, which showed a single EMG burst, EMG patterns consisted of two or three progressively larger components occurring reciprocally in antagonistic muscles. Increasing walking speed yielded a significant reduction of the activity in distal muscles, and a simultaneous increment in proximal muscles. The mechanical effect of the earlier braking actions, estimated from the backward-directed wave of the horizontal ground reaction force, decreased in a velocity-dependent manner. In the swing limb the braking activities began approximately 330 ms after the stop signal and, on average, revealed a proximal-to-distal activation sequence with the extensor groups (quadriceps, QUAD, and SOL) playing a prominent role. They always consisted of single EMG bursts, largely co-activated in the antagonist muscles. The onset latencies of the individual components showed a close correlation, and the spatio-temporal parameters were always scaled in parallel. Unlike the stance limb, the mechanical braking action associated with the final contact of the swing limb increased with walking speed. The results indicate that the muscle synergies responsible for the rapid termination of gait in response to a ground-contact visual cue are produced by a relatively flexible set of motor commands modulated according to different velocity-dependent strategies in the weight-bearing limb, and by a single, fairly robust motor programme in the swing limb. Mechanical constraints related to the relative position of the centre of foot pressure and centre of body mass at the time the braking commands begin to affect external forces, may condition the difference between the two sides of the body. Most of the available information on the physiology of locomotor control comes from studies performed under steady-state walking conditions. Among non-stationary locomotor behaviours, the initiation of gait has been examined in some detail (Carsloo, 1966; Herman et al. 1973; Breniere et al. 1981; Breniere & Do, 1987; Crenna et al. 1990; Crenna & Frigo, 1991a; Lepers & Breniere, 1995; Halliday et al. 1998). However, the opposite motor task (i.e. the transition from constant-speed walking to static postural attitudes) has received little attention. Investigation of the neural basis of the termination of gait in freely moving animals has shown that the activation of central areas located close to those involved in gait onset (e.g. the dorsal tegmental field of the caudal pons) can slow down and eventually stop spontaneous walking (Mori et al. 1989). The effects were ascribed to a partial withdrawal of descending facilitatory drives to the antigravity muscles and to active inhibition of the propulsive activity (Mori, 1987). Indirect insight into the mechanisms underlying the termination of gait in humans was obtained by measuring biomechanical variables such as ground reaction forces and relative trajectories of the centre of body mass (CM) and the centre of foot pressure (CP). The results of such studies demonstrate the contribution of ‘negative’ effects, reflected in the depression of the vertical and forward-directed ground reaction forces during propulsive phases, and ‘positive’ braking phenomena, evidenced by increased vertical and backward-directed reaction forces during body weight loading (Yamashita & Katoh, 1976; Jaeger & Vanitchatchavan, 1992). In the presence of favourable foot positioning, these two complementary actions cause displacement of the CP ahead of CM, leading to deceleration of the body (Jian et al. 1993). By means of a different protocol, whereby walking was abruptly interrupted in response to a strong cutaneous stimulation (to simulate hitting an obstacle), Hase & Stein (1998) obtained EMG confirmation of the intervention of negative and positive mechanisms. According to the current notion, therefore, the termination of human gait is achieved by switching off the ongoing locomotor output, but it can also involve various excitatory actions that are bound to interfere with the current movement. In this respect the braking commands appear to operate as discrete self-paced perturbations, particularly at higher walking speeds, on account of the acceleration-dependent inertial load to be counteracted and the inherent unsteadiness of bipedal progression (Adamovich et al. 1994; Taga, 1995). The characteristics of this commonplace motor task, entailing potentially destabilising interactions between voluntary (stopping) and mainly automatic (locomotor) commands, render the termination of gait an interesting topic in the field of motor control physiology, and raise a number of basic issues that have not been dealt with before. In the first place there is an obvious need for understanding in some detail the spatial and temporal organisation of the muscle activities responsible for deceleration in the weight-supporting limb and the swing limb. The modalities of interaction between the excitatory actions and the ongoing locomotor rhythm need to be elucidated, as do the associated mechanical effects. Moreover, the strategies adopted by the nervous system for tuning the braking commands in relation to walking speed still await analysis. The present study sought to address these questions in order to provide a functional characterisation of the motor programmes responsible for the termination of human gait in one of the most natural conditions, i.e. in response to visual cues.