Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans

Abstract

Objective: Manipulation of afferent input can induce reorganization within the sensorimotor cortex which may have important functional consequences. Here we investigate whether prolonged peripheral nerve stimulation can induce reorganization within the human motor cortex.

Methods: Using transcranial magnetic stimulation, we mapped the scalp representation of the corticospinal projection to hand muscles in 8 normal subjects before and after 2 h of simultaneous repetitive electrical stimulation of the ulnar and radial nerves at the wrist. Control mapping experiments were conducted in 6 subjects.

Results: Following nerve stimulation, larger motor-evoked potentials were evoked from more scalp sites. The induced changes were most apparent in first dorsal interosseous, but were also seen in other hand muscles. The increases in area of the representational maps were accompanied by changes in the location of the optimal site for evoking responses in first dorsal interosseous, and changes in the centres of gravity of the maps.

Conclusions: Prolonged afferent stimulation induces an increase in excitability of the corticospinal projection. This is accompanied by a significant shift in the centre of gravity of the stimulated muscles which we propose is evidence of a non-uniform expansion in their cortical representation.

Introduction

The organization of the sensorimotor cortex is not fixed and many external manipulations can produce organizational changes within these regions. Stereotyped afferent inputs appear to be a key factor in producing these organizational changes. There are many examples of altered patterns of afferent input inducing organizational cortical change. Zarzecki et al. (1993) demonstrated that when digit 4 was removed or joined with digit 3, the incidence of excitatory post-synaptic potentials increased dramatically in digit 4's sensory cortical representational zone with stimulation of adjacent digits. Electrical stimulation of peripheral nerves also increases the receptive field size of cells in the sensory cortex. In cats, Recanzone et al. (1990) demonstrated that within 1–2 h of electrical stimulation of a cutaneous nerve, the sensory cortical representation of the territory innervated by that nerve increased at least in the short term. Comparable findings have been reported in the motor cortex. Amputation of the forelimb in rats results in marked reorganization within the motor cortex with the adjacent vibrissae and shoulder representations expanding into the former forelimb territory (Donoghue and Sanes, 1988).

Until recently, it was possible to obtain a map of the motor cortex only during neurosurgical procedures. However, it is now possible to obtain a functional representation of the corticospinal projection to a variety of muscles by using transcranial magnetic stimulation (TCMS) to activate the motor cortex at a number of scalp sites. These maps represent activation of the primary motor cortex (Wassermann et al., 1996) and it is possible to obtain useful somatotopic information using this technique (Wassermann et al., 1992, Wilson et al., 1993). TCMS studies have demonstrated that manoeuvres which inter alia alter sensory input can induce organizational change within the motor cortex. For example, following amputation (Cohen et al., 1991, Ridding and Rothwell, 1995) and ischaemic nerve block (Brasil-Neto et al., 1992), motor evoked potentials (MEPs) in muscles proximal to the amputation or block are larger, and can be evoked from a greater number of scalp sites than responses in homologous muscles in the intact limb. Repetitive movements also lead to an increase in MEP amplitude in muscles involved in the task (Pascual-Leone et al., 1995). It has been recently reported that a period of repetitive electrical stimulation of peripheral nerves can induce an increase in the amplitude of MEPs evoked by TCMS in muscles innervated by the stimulated nerve (Ridding et al., 2000). This study also suggested that following peripheral stimulation there might also have been a shift in the cortical representational zones of the target muscle.Here we investigate whether changes in cortical excitability following a period of peripheral nerve stimulation are accompanied by expansion or reorganization of the motor map. Our findings confirm that a period of prolonged peripheral stimulation induces excitability changes in the corticospinal projection to hand muscles, and that these changes are accompanied by significant reorganization with enlargement of the scalp evoked motor maps.