Contribution of afferent feedback and descending drive to human hopping

Abstract

During hopping an early burst can be observed in the EMG from the soleus muscle starting about 45 ms after touch-down. It may be speculated that this early EMG burst is a stretch reflex response superimposed on activity from a supra-spinal origin. We hypothesised that if a stretch reflex indeed contributes to the early EMG burst, then advancing or delaying the touch-down without the subject's knowledge should similarly advance or delay the burst. This was indeed the case when touch-down was advanced or delayed by shifting the height of a programmable platform up or down between two hops and this resulted in a correspondent shift of the early EMG burst. Our second hypothesis was that the motor cortex contributes to the first EMG burst during hopping. If so, inhibition of the motor cortex would reduce the magnitude of the burst. By applying a low-intensity magnetic stimulus it was possible to inhibit the motor cortex and this resulted in a suppression of the early EMG burst. These results suggest that sensory feedback and descending drive from the motor cortex are integrated to drive the motor neuron pool during the early EMG burst in hopping. Thus, simple reflexes work in concert with higher order structures to produce this repetitive movement.

Figure 3. Averaged time points during hopping with time 0 indicating the crossing of the light barrier

The white background indicates the moving platform protocol. ‘Up’, ‘Level’ and ‘Down’ refer to the position of the platform. The grey background indicates the TMS protocol, ‘Control’ refers to unstimulated trials and ‘TMS’ refers to trials with a subthreshold TMS stimulus. Error bars at the start and end of the bar indicate the s.e.m. of the time of that event relative to the crossing of the light barrier, while the numbers written in the bar indicate the time between the events ±s.e.m.A, the timings of touch-down detected by the vertical force on the platform ±s.e.m. In B the beginning of the bar shows the time of and the end indicates peak of the early EMG burst and thus the length of the bar indicates the duration between those events. It can be seen that the time between and the peak of the early EMG burst remains the same in the three conditions. Only the time of is displayed in the stimulated condition of the TMS protocol since the position of the peak is concealed by the after-effects of the suppression. In C‘TMS stimulus’ indicates the time point where the TMS stimulus is delivered. ‘Suppression’ represents the average timing and duration of the suppression. By comparing it with the control condition in Fig. 3B), it can be seen that the suppression is timed just prior to the peak of the early EMG burst.

Figure 1. Raw and ensemble averaged EMG and kinematics during hopping in a single subject

A, raw EMG and kinematics from three hops. ▾ indicates an artefact in the force signal due to acceleration and deceleration of the platform. ♦ indicates the point where the ankle angle shows a maximal dorsiflexion acceleration . B, ensemble average of 25 sweeps for the conditions ‘Up’, ‘Level’ and ‘Down’. All averaged trials are aligned to the crossing of the light barrier. Note that the platform in the ‘Up’ position causes a shift in the signals for ankle angle, ground reaction force and the EMG burst in SOL ahead in time whereas the ‘Down’ position delays these signals in time.

Figure 2. Correlation between the shift in() and the peak of the EMG burst ()

Each subject is represented by two data points, one for platform up and one for platform down. Positive numbers indicate the situation in which the event ( or EMG peak) is delayed compared to the level position (platform down); negative numbers are situations in which those events are shifted ahead (platform up).

Figure 4. TMS-evoked EMG suppression during the early EMG burst

A, ensemble averaged EMG and kinematic data (80 sweeps) of the stimulated and unstimulated condition from a single subject showing a TMS-evoked EMG suppression in SOL, GM and TA (shaded). Time 0 is aligned with ground contact. B, the same data zoomed in the x-direction. The dashed line indicates the time of the TMS stimulus and the dotted line the onset of suppression.