Phase-dependent and task-dependent modulation of stretch reflexes during rhythmical hand tasks in humans

Abstract

Phase-dependent and task-dependent modulation of reflexes has been extensively demonstrated in leg muscles during locomotory activity. In contrast, the modulation of reflex responses of hand muscles during rhythmic movement is poorly documented. The objective of this study was to determine whether comparable reflex modulation occurs in muscles controlling finger motions during rhythmic, fine-motor tasks akin to handwriting. Twelve healthy subjects performed two rhythmic tasks while reflexes were evoked by mechanical perturbations applied at various phases of each task. Electromyograms (EMGs) were recorded from four hand muscles, and reflexes were averaged during each task relative to the movement phase. Stretch reflexes in all four muscles were found to be modulated in amplitude with respect to the phase of the rhythmic tasks, and also to vary distinctly with the tasks being conducted. The extent and pattern of reflex modulation differed between muscles in the same task, and between tasks for the same muscle. Muscles with a primary role in each task showed a higher correlation between reflex response and background EMG than other muscles. The results suggest that the modulation patterns observed may reflect optimal strategies of central-peripheral interactions in controlling the performance of fine-motor tasks. As with comparable studies on locomotion, the phase-dependency of the stretch reflexes implies a dynamically fluctuating role of proprioceptive feedback in the control of the hand muscles. The clear task-dependency is also consistent with a dynamic interaction of sensory feedback and central programming, presumably adapted to facilitate the successful performance of the different fine-motor tasks.

Figure 1. Photograph of the apparatus and experimental setup with a subject participating

Illustration of the protocol showing the task ‘rhythmic pen squeezing’ (RPS). The same actuator was used in both rhythmical tasks of this study.

Figure 2. Original record showing the constancy of the mechanical stimuli, randomly applied at different phases of the movement cycle

Recordings of the mechanical stimulus pulses (S), the perturbations applied to the pen-tip (P), the force exerted by the index finger on the force-measuring pen (F), and (lower traces) the concurrent raw EMGs in the four hand muscles as indicated, during the rhythmic pen squeezing task in one subject. The mean velocity of the applied stretches was 5.505 ± 0.282 m s⁻¹ (s.d.), ranging from 4.97 to 5.79 m s⁻¹. FDI, first dorsal interosseous; FDS, flexor digitorum superficialis; EPB, extensor pollicis brevis; FPB, flexor pollicis brevis.

Figure 3. Reflex responses evoked by mechanical stimuli during a rhythmic task in a typical subject

Reflex EMG responses elicited in four hand muscles during the rhythmic pen squeezing task in one subject. Each of the four traces represents an average of approximately 200 sweeps, irrespective of the phase in which the stimuli occurred. Stimuli were applied at time zero as indicated by arrow (S).

Figure 4. Phase-dependency of reflex responses at various phases of a cyclical finger movement

A, modulation of FDI reflex responses evoked in 8 successive phases of the full task cycle during rhythmic finger abduction in one subject. Each trace represents the average of the individual responses to approximately 25 stimuli occurring in the phase indicated on the left. B, average of background EMG over the full cycle, and resultant force exerted by the index finger, aligned vertically in relation to the 8 phases shown in A. Force: arbitrary units (increasing towards the right).

Figure 5. Patterns of phase-dependency of reflex modulation compared with background EMG cycle

Modulation of reflex EMG responses elicited in FDI and FDS as a function of the phase of two rhythmic hand tasks, compared with background EMG activity, obtained in all 12 subjects. A and B, average of reflex response and background EMG activity in 8 equal phases for the RFA (rhythmic finger abduction) task in FDI and FDS. C and D, average of reflex response and background EMG activity in 16 equal phases for the RPS (rhythmic pen squeezing) task in FDI and FDS.Y-axis on the left of each graph shows mean reflex amplitude for each phase; secondary Y-axis on the right represents background EMG (normalized). Error bars (s.e.m.) are for reflex responses (omitted from background EMG for clarity).

Figure 6. Task-dependency of reflex modulation as a function of background EMG activity

Relationship between the reflex EMG response and normalized background EMG for the tasks RFA (rhythmic finger abduction) and RPS (rhythmic pen squeezing) in muscles FDI and FDS, averaged across 12 subjects. A, correlations and regression lines for FDI in tasks RFA (o, r²= 0.896, slope k= 100.14 ± 17.88) and RPS (▴, r²= 0.708, slope k= 59.76 ± 6.99). The difference in slope is statistically significant between the tasks (P < 0.05). B, correlations and regression lines for FDS in tasks RFA (•, r²= 0.273, slope k= 22.55 ± 3.49) and RPS (Δ, r²= 0.525, slope k= 123.27 ± 8.43). The difference in slope is also significant (P < 0.01). Standard errors are omitted for clarity (see Fig. 5).