Early somatosensory processing during tonic muscle pain in humans: relation to loss of proprioception and motor ‘defensive’ strategies

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Abstract

Objective: It is known that tonic muscle pain induced by a Levo-Ascorbic (L-AS) solution injected in a foot muscle can transiently modify both regional proprioception and stimulus perception. These findings are paralleled by changes of middle-latency lower-limb somatosensory evoked potentials (SEPs). However, little is known on the behaviourally relevant aspect whether eventual SEP pain-induced changes could be partly due to a sort of ‘motor strategy’ of subjects in the frame of a self-protective reaction towards the noxious stimulus. Movement and imagery of movements are in fact known to reduce mainly pre-central SEP amplitude (i.e. gating effect).

Methods: Low-threshold afferents ulnar SEPs, psychophysical pain ratings and fingers’ position sense were monitored in the time-course during L-AS injection in the right first dorsal interosseous muscle. Control experiments included SEPs (either following prevalent ulnar nerve low-threshold afferent stimulation or more conventional mixed nerve stimulation) during actual movements execution and imagery of movements of the right hand.

Results: Tonic pain induced a significant reduction of the post-central N20-P25-N33 complex and a significant increase of the N18 wave. These changes, that were paralleled by distortion of the finger position sense, were delayed 2–5 min with respect to the maximal subjective pain sensation. Conversely, movement imagery tasks lead to a significant, selective, reduction of the pre-central N30 complex. This wave was even more reduced during actual movements, in combination with a reduction of those post-central components peaking after the first activation of the primary sensory cortex.

Conclusions: Early sensory processing at cortical level is changed during tonic muscle pain, mainly for those components which may be theoretically involved in proprioceptive afferent elaboration. These changes are likely not due to subconscious or voluntary motor strategies of the subjects in the frame of a self-protective aversive reaction towards the noxious stimulus.

Introduction

Two peripheral stimuli belonging to different sub-modalities within the somatic domain, when delivered concurrently, may be perceived differently from the same stimuli when presented separately: indeed, superimposed discharges from separate peripheral sources can interact to produce spatial facilitation, occlusion or inhibition (Kang et al., 1985). Recent examples in humans indicate that muscle pain may modify central transmission of proprioceptive segmental (Rossi and Decchi, 1995, Rossi and Decchi, 1997, Rossi et al., 1998) and supraspinal pathways (Capra and Ro, 2000). Chemically-induced tonic muscle pain from foot muscles (Rossi and Decchi, 1995, Rossi and Decchi, 1997) alters foot position sense as well as the capability to identify an electrical stimulus adjusted for the stimulation of foot proprioceptive afferent fibres (Rossi et al., 1998). At cortical level, these pain-induced psychophysical changes are paralleled by a selective decrease of middle-latency components of lower limb somatosensory evoked potentials (SEPs) (Rossi et al., 1998). These findings and the observation of an increased parietal delta and alpha-1 bands power (Le Pera et al., 2000) during tonic pain, are consistent with the classical experimental observation of a decreased responsiveness/excitability of the sensory cortex during nociceptive discharges (Melzack and Casey, 1968).

The first aim of the current study was to verify whether proprioceptive SEP changes observed during muscle nociceptive stimulation of the foot could be also detected during similar nociceptive stimulation applied to hand muscles. This might have relevance for different reasons.

(1) It is not obvious that proprioceptive and nociceptive interactions from the upper limb are the same described from the lower limb. It has been shown, for example, that flexor reflex interneuronal system subserving pain input from the foot is subjected to load-dependent modulation which is aimed to protect stance and gait stability (Decchi et al., 1997).

(2) Cortical generators of upper limb SEP are better detailed than those of lower limb, at least in the early phases (i.e., 20–40 ms) of the sensory processing; therefore, eventual pain-induced SEP changes could provide further insights on cortical processing and elaboration of proprioceptive sensory information when superimposed to a tonic nociceptive discharge coming from the same muscle.

A second aim was to explore an additional putative mechanism which could be in part responsible for those SEP pain-induced changes already described at lower limb: tonic nociceptive muscle stimulation could, in fact, promote the elaboration of a cortical motor plan containing a self-protective reaction towards the noxious stimulus. Notably, the motor cortical output, as tested with transcranial magnetic stimulation, seems to be inhibited during tonic pain (Le Pera et al., 2001). Such ‘motor strategy’ could per se modify cortical sensory processing. This represents a behaviourally relevant aspect, but it has been poorly addressed in previous electrophysiological and neuroimaging studies (Hsieh et al., 1994, Porro et al., 1998, Rossi and Decchi, 1997, Rossi et al., 1998, Le Pera et al., 2000, Le Pera et al., 2001) dealing with tonic muscle pain in humans. Hence, ad hoc experiments were designed using actually executed and imagined hand movements as conditionings: both tasks are known to produce amplitude reduction of the pre-central N30 SEP complex and, to lesser extent, of the parietal components following the N20 wave, reflecting possible centrifugal gating mechanisms of the incoming sensory flow (Cohen and Starr, 1987, Rossini et al., 1990, Rossini et al., 1996, Rossini et al., 1997, Cheron and Borenstein, 1987, Cheron and Borenstein, 1992, Kristeva-Feige et al., 1996, Hallett, 2000, Rossi et al., 2002).

Section snippets

Subjects and methods

Thirteen healthy volunteers (age range 26–40 years, 8 males and 5 females), all right-handed, underwent neurophysiological investigations after the approval of the entire protocol by the local ethics committee. Subjects lay on a reclining chair in a quiet room, with forearms resting on armchairs. In order to avoid cutaneous interference during stimulation at palm and digit levels, the right hand rested pronated outside the armchair.

Brain responses were recorded with a commercially available

Behavioural findings during and following tonic pain

Psychophysical curves of pain showed that the maximal peak pain was consistently reached after about 2 min from the L-AS injection; then, after a plateau phase lasting about 2 min, it progressively decreased in the following minutes, and vanished after about 17–20 min (Fig. 1).

The pain was qualitatively described as deep burning or compressive, involving almost the whole hand. Most subjects complained of a cramp-like sensation in the FDI, often spreading to other interossei muscles.

Discussion

Results from the present study confirm and add new insights to previous findings on lower-limb SEPs during tonic muscle pain (Rossi et al., 1998). Reduction of post-central complex N20-P25-N33 and increasing of the far-field N18 wave, with unchanged post-central N20 and pre-central P22-N30 components were consistently observed. All these changes had a time-course parallel to the subjective pain rating curve, indicating a clear-cut interaction between muscle nociceptive discharge and sensory

Acknowledgements

The authors thank Mr. Benito Vecchiarelli for excellent assistance during SEP recordings.

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