Modulation of flexion reflex induced by hip angle changes in human spinal cord injury

Abstract

The flexion reflex can be elicited via stimulation of skin, muscle, and high-threshold afferents inducing a generalized flexion of the limb. In spinalized animal models this reflex is quite prominent and is strongly modulated by actions of hip proprioceptors. However, analogous actions on the flexion reflex in spinal cord injured (SCI) humans have not yet been examined. In this study, we investigated the effects of imposed static hip angle changes on the flexion reflex in ten motor incomplete SCI subjects when input from plantar cutaneous mechanoreceptors was also present. Flexion reflexes were elicited by low-intensity stimulation of the sural nerve at the lateral malleolus, and were recorded from the ipsilateral tibialis anterior (TA) muscle. Plantar skin stimulation was delivered through two surface electrodes placed on the metatarsals, and was initiated at different delays ranging from 3 to 90 ms. We found that non-noxious sural nerve stimulation induced two types of flexion reflexes in the TA muscle, an early, and a late response. The first was observed only in three subjects and even in these subjects, it appeared irregularly. In contrast, the second (late) flexion reflex was present uniformly in all ten subjects and was significantly modulated during hip angle changes. Flexion reflexes recorded with hip positioned at different angles were compared to the associated control reflexes recorded with hip flexed at 10 degrees. Hip flexion (30 degrees, 40 degrees) depressed the late flexion reflex, while no significant effects were observed with the hip set in neutral angle (0 degrees). Strong facilitatory effects on the late flexion reflex were observed with the hip extended to 10 degrees. Moreover, the effects of plantar skin stimulation on the flexion reflex were also found to depend on the hip angle. The results suggest that hip proprioceptors and plantar cutaneous mechanoreceptors strongly modulate flexion reflex pathways in chronic human SCI, verifying that this type of sensory afferent feedback interact with spinal interneuronal circuits that have been considered as forerunners of stepping and locomotion. The sensory consequences of this afferent input should be considered in rehabilitation programs aimed to restore movement and sensorimotor function in these patients.

Fig. 1

The full-wave rectified EMG averages of the two classes of the flexion reflex are identified by vertical cursors placed at the start and at the end of the corresponding EMG burst. For all three subjects, the top EMG corresponds to the stimulation intensity during which a response in the tibialis anterior muscle was first observed. In subject 10 (c), the early flexion reflex was absent when the sural nerve was stimulated at non-nociceptive stimulus intensities

Fig. 2

Effects of imposed static hip angle changes on the late flexion reflex.(a) The average late flexion reflex recorded with the ipsilateral hip set at 10° of flexion (control hip angle), 30° of flexion, 40° of flexion and at 10° of extension for one subject (s7) is presented. (b) Pool data showing the effects of hip angle variations on the late flexion reflex. For each hip angle tested, the average size of the conditioned late flexion reflexes (as a percentage of the control late flexion reflex recorded with hip flexed at 10°) was calculated for all subjects tested. Asterisks indicate cases of statistically significant differences between the control and the conditioned reflex sizes (P<0.05). Error bars indicate the SEM

Fig. 3

Time course of the effects of plantar cutaneous afferent excitation on the late flexion reflex with hip positioned at 10° of extension (a), 10° of flexion (b), and at 30° of flexion (c). For each conditioning test interval, the overall average size of the conditioned late flexion reflex is presented as a percentage of the associated control flexion reflex recorded at each hip angle tested. Asterisks indicate statistically significant differences between the conditioned and the control flexion reflex (P<0.05). Error bars represent the SEM