Selective gating of lower limb cortical somatosensory evoked potentials (SEPs) during passive and active foot movements

Abstract

We evaluated subcortical and cortical somatosensory evoked potentials (SEPs) in response to posterior tibial nerve stimulation in 4 experimental conditions of foot movement and compared them with the baseline condition of full relaxation. The experimental conditions were: (a) active flexion-extension of the stimulated foot; (b) active flexion-extension of the non-stimulated foot; (c) passive flexion-extension of the stimulated foot in complete relaxation; (d) tonic active flexion of the stimulated foot. We analyzed latencies and amplitudes of the subcortical P30 potential, of the contralateral pre-rolandic N37 and P50 responses and of the P37, N50 and P60 potentials recorded over the vertex. Latencies did not vary in any of the paradigms. The amplitude of subcortical P30 potential did not change during any of the paradigms. Among the cortical waves, P37, N50 and P60 amplitudes were significantly attenuated in all conditions except active movement of the non-stimulated foot (b). This attenuation was less during passive (c) than during active movements of the stimulated foot (a and d). The contralateral pre-rolandic waves N37 and P50 showed no significant decrease during any of the paradigms. These results suggest that gating occurs rostrally to the cervico-medullary junction, probably at cortical level. The different behavior of N37, P50 and P37, N50 cortical responses during movement of the stimulated foot provides evidence suggestive of a highly localized gating process occurring at cortical level. These potentials could reflect activation of separate, functionally distinct generators.

Introduction

Somatosensory evoked potentials (SEPs) studies in humans have documented that the transmission of afferent information along the somatosensory pathway is gated during movement of the corresponding body part (Rushton et al., 1981; Cohen and Starr, 1985; Cohen and Starr, 1987; Seyal et al., 1987; Cheron and Borenstein, 1987; Jones et al., 1989; Rossini et al., 1990; Cheron and Borenstein, 1991; Huttunen and Homberg, 1991; Cheron and Borenstein, 1992; Weerasinghe and Sedgwick, 1994; Rossini et al., 1996). This gating seems to be largely dependent on the nature of the movement. Passive movement produces cortical SEPs attenuation which has been attributed to afferent occlusive mechanisms (centripetal gating) (Rushton et al., 1981; Jones et al., 1989), while cortical SEPs suppression during voluntary movement have been mainly attributed to efferent motor control over somatosensory input processing pathway (centrifugal gating) (Cohen and Starr, 1987; Cheron and Borenstein, 1991).

Whereas these mechanisms have been extensively investigated for upper limb SEPs during different kinds of finger movements (Rushton et al., 1981; Cohen and Starr, 1987; Seyal et al., 1987; Cheron and Borenstein, 1987; Jones et al., 1989; Rossini et al., 1990; Cheron and Borenstein, 1991; Huttunen and Homberg, 1991; Cheron and Borenstein, 1992; Weerasinghe and Sedgwick, 1994; Rossini et al., 1996), only a limited number of studies have been performed to evaluate the effect of movement on lower limb SEPs (Cohen and Starr, 1985; Seyal et al., 1987).

Cohen and Starr (1985)reported that tonic flexion of the foot during stimulation of the ipsilateral posterior tibial nerve attenuated cortical responses P1, N1 recorded over the vertex, without affecting the segmental lumbar response. Similar SEP patterns were later described by Seyal et al. (1987)during active movement of the foot, suggesting that this modulation occurs rostrally to the level of the lumbo-sacral cord.

However, these studies did not permit to establish whether this central modulation occurs in the intraspinal, or intracranial segment of the somatosensory pathway since the scalp P30 potential which originates in the lower brainstem (Urasaki et al., 1993; Tinazzi et al., 1996a; Tinazzi et al., 1996b) was not recorded.

Furthermore, these studies have evaluated only the so-called `W' shaped cortical complex (P37-N50-P60) recorded at the Cz electrode site using a midfrontal reference montage. This montage is inadequate for the separate study of P37, N50 and contralateral frontal N37, P50 responses which could be generated by distinct generators in the primary somatosensory cortex (Beric and Prevec, 1981; Vas et al., 1981; Pelosi et al., 1988; Tinazzi et al., 1996a).

In the present study we recorded cortical and subcortical tibial and sural nerve SEPs during different experimental protocols of foot movement (passive, active foot movement and isometric contraction).

Our aims were: first, to investigate whether gating processes produce selective attenuation of cortical P37, N50 potentials and of contralateral frontal N37, P50 potentials; second, to address the question whether changes of subcortical neural activity could account for the gating of cortical responses.