Time-related changes of excitability of the human motor system contingent upon immobilisation of the ring and little fingers

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Abstract

Objectives: To examine possible changes of excitability of the human motor system contingent upon immobilisation of two hand fingers.

Methods: Two series of 5 transcranial magnetic stimulation (TMS) sessions were carried out on different days (1, 2, 3, 4, and 7). In one series (fingers immobilised, FI), subjects wore for 4 days a device that kept immobilised the left fourth and fifth finger. In the other series (fingers free, FF), no constraining device was used. Focal TMS was applied over the right motor cortex and motor evoked potentials (MEPs) were recorded from left abductor digiti minimi (immobilised) and first dorsal interosseus (non-immobilised) muscles. Intensities of 10, 30, and 50% above the resting motor threshold (rMT), were used.

Results: In FI series, rMT for both muscles showed significant increase on days 3, 4, and 7 with respect to day 1. At high stimulation intensity a clear decrease of MEPs amplitude was observed on days 3 and 4 for both muscles. Since no time-related changes of peripheral (M-wave) and spinal (F-wave) excitability were noted, MEPs and rMT changes are likely to have a cortical origin. In FF series, no changes of excitability were detected.

Conclusions: Sensorimotor restriction of two fingers induces an early decrease of excitability, possibly at cortical level, which involves not only the immobilised muscle but also muscles with purportedly overlapping neural representations.

Introduction

Convergent evidence from research in animals and humans indicates that physiological or pathological perturbations of somatic input and motor output may induce major neuroplastic changes at different levels of the somatosensory and motor system even in adults (Jones, 2000, Sanes and Donoghue, 2000). These changes have been documented by using two main approaches. The first approach includes models in which neural changes are observed as consequence of an increase of sensory input and motor output (Jenkins et al., 1990, Recanzone et al., 1992b, Wang et al., 1995, Xerri et al., 1999). Learning the sensorimotor skills necessary for reproducing motor sequences on a piano keyboard, for example, brings about an increase of the neural representation of the body parts that perform the task (Pascual-Leone et al., 1995a). An expansion of the neural representation of the working hand has also been observed in subjects who practice highly specialised sensorimotor activities such as playing violin or reading Braille (Elbert et al., 1995, Pascual-Leone et al., 1995b). The second approach includes models in which neural changes are observed as a consequence of decrease of sensory input and/or motor output (Kaas, 2000). Neurophysiology and functional imaging studies provide evidence for remapping processes contingent upon a reduction of somatosensory input and motor output in amputee monkeys (Pons et al., 1991, Florence and Kaas, 1995, Qi et al., 2000), in humans (Cohen et al., 1991, Elbert et al., 1994, Kew et al., 1994, Pascual-Leone et al., 1996), and in patients with short- or long-lasting peripheral deafferentation (Rossini et al., 1996, Tinazzi et al., 1997, Tinazzi et al., 1998). Even less is known on neural changes in the central nervous system contingent upon disuse in normal humans. Indeed, the majority of studies, in which immobilisation of a given body part is used, mainly examine changes of the properties of muscles or motor units (Seki et al., 2001a, Seki et al., 2001b). Two recent studies used transcranial magnetic stimulation (TMS) to map the motor representation of muscles in non-brain-damaged subjects who wore casts because of fractures of the wrist (Zanette et al., 1997) or the leg (Liepert et al., 1995), either on the left or the right side. Areal extension of motor maps for cast immobilised and non-immobilised muscles provided indices of neural changes in the human motor system contingent upon the sensorimotor restriction procedure. It is puzzling that these two studies, conducted by means of the very same technique and very similar mapping procedures, provided conflicting results. The first study found that the areal extent of motor maps of long-term immobilised muscles (for at least 4 weeks) shrinks with respect to the homologous, contralateral, non-immobilised muscles (Liepert et al., 1995). By contrast, the second study, carried out in patients with immobilisation of upper limbs due to bone fractures, found a volumetric increase of motor maps of the immobilised muscles (Zanette et al., 1997).

The present study deals with the controversial issue of the effects of disuse on the excitability of the motor system in humans by using TMS. This technique is used with the aim of assessing possible modifications of cortical, spinal, and peripheral excitability contingent upon motor restriction of two fingers of the non-dominant hand. Moreover, the present research is aimed at providing novel evidence on the relationship between immobilisation and changes of excitability at different levels of the motor system, by also addressing two issues, which have never been addressed hitherto. The first issue concerns the time course of possible neural changes induced by disuse. Indeed, previous studies on the effect of immobilisation in normal humans reported that changes of neural excitability occurred weeks or even months after the beginning of the immobilisation. It is worth noting that the immobilisation procedure induces dramatic modifications of sensorimotor behaviour as soon as the cast is applied. Thus, changes of neural excitability may appear much earlier than previously believed. Theoretically, these changes may be detected in the central nervous system, either at cortical or subcortical levels, even before changes in the peripheral nerve and muscle are observed. At variance from previous studies, not only do we provide indices of neural activity before immobilisation but also specifically look for early changes of motor excitability in the immobilised muscles.

The second issue is concerned with whether changes of motor excitability are selective for the immobilised muscles or extend to muscles with at least partially separate neural representation. Studies of use-dependent plasticity in animals show that increases of neural representation may involve the trained part rather selectively (Kleim et al., 1998, Nudo et al., 1996, Recanzone et al., 1992a, Recanzone et al., 1992b). Moreover, the increase of neural representation in Braille readers who extensively used the right index finger did not extend to the non-active right little finger (Pascual-Leone et al., 1995b). No comparable data are available from sensorimotor restriction studies whereby changes of excitability of the immobilised muscles are typically compared with homologous muscles on the opposite side and hemisphere (Liepert et al., 1995, Zanette et al., 1997). In the present study, we recorded motor evoked potentials (MEPs) not only from the constrained abductor digiti minimi (ADM) but also from the non-constrained first dorsal interosseus (FDI) of the same hand. Thus, the two targeted muscles are not only represented in the same hemisphere but they may also have, like other intrinsic muscles of the hand, at least partially overlapping neural representation (Lewko et al., 1996, Wilson et al., 1993).

Section snippets

Subjects

Eleven healthy subjects (4 men and 7 women) gave their written informed consent to participate in the study. The local ethical committee approved the protocol. All subjects were right handed according to the Handedness Edimburgh Inventory (Oldfield, 1971). Their mean age was 28.3 (SD=6.2, range 23–48). Six subjects were aware of the purposes of the study.

Each subject took part in two different experimental conditions carried out at least at an interval of 1 month. Each condition consisted of 5

Statistical analysis

rMT values and average values of MEPs, F- and M-waves were submitted to 4 separate analysis of variances (ANOVAs) with repeated measures. The main factors of each analysis were the following: conditions (FI and FF); muscles (ADM, FDI); and days (1, 2, 3, 4, and 7). ANOVAs on amplitude of MEPs had the additional factor of intensity of stimulation (10, 30, and 50% above rMT). Post hoc comparisons were performed by using Tukey's honest significant differences test.

Results

Location of OSP was on average comparable in the two experimental conditions being located: 4.9 cm (SD 1.02) ahead and 2.9 cm (SD 0.67) laterally from Cz in the FI condition; and 4.8 cm (SD 1) ahead and 3.1 cm (SD 0.92) laterally from Cz in the FF condition.

Analysis of rMT in the FI condition showed that the factor day was significant (F(1,10)=6.388, P=0.0005). This effect has to do with the increase of rMT over the different days (Fig. 2, left part of the figure). Post hoc tests revealed that rMT

Discussion

The major finding of the present study is that a short-term motor restriction of two fingers of the non-dominant hand brings about changes of MEP amplitudes and rMT which indicate a decrease of cortical excitability of the restricted muscle and of a non-restricted muscle of the same hand. It is relevant that no changes of excitability were detected in the FF conditions, thus indicating that changes observed in FI conditions were specifically related to the restriction procedure.

Acknowledgements

This work was supported by grants from the Human Frontier Science Program (RG 0161/1999-B) and COFIN 2000, to S.M.A. We wish to thank Mr Marco Veronese for his technical help.

References (51)

  • P.M Rossini et al.

    Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee

    Electroenceph clin Neurophysiol

    (1994)
  • P.M Rossini et al.

    Focal brain stimulation in healthy humans: motor maps changes following partial hand sensory deprivation

    Neurosci Lett

    (1996)
  • M Tinazzi et al.

    Transient deafferentation in humans induces rapid modulation of primary sensory cortex not associated with subcortical changes: a somatosensory evoked potential study

    Neurosci Lett

    (1997)
  • S.A Wilson et al.

    Transcranial magnetic stimulation mapping of the motor cortex in normal subjects. The representation of two intrinsic hand muscles

    J Neurol Sci

    (1993)
  • G Zanette et al.

    Reversible changes of motor cortical outputs following immobilization of the upper limb

    Electroenceph clin Neurophysiol

    (1997)
  • T Allard et al.

    Reorganization of somatosensory area 3b representations in adult owl monkeys after digital syndactyly

    J Neurophysiol

    (1991)
  • S.A Clark et al.

    Receptive fields in the body-surface map in adult cortex defined by temporally correlated inputs

    Nature

    (1988)
  • L.G Cohen et al.

    Motor reorganization after upper limb amputation in man (a study with focal magnetic stimulation)

    Brain

    (1991)
  • H Devanne et al.

    Input–output properties and gain changes in the human corticospinal pathway

    Exp Brain Res

    (1997)
  • A Eisen

    Electromyography in disorders of muscle tone

    Can J Neurol Sci

    (1987)
  • T Elbert et al.

    Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury

    NeuroReport

    (1994)
  • T Elbert et al.

    Increased cortical representation of the fingers of the left hand in string players

    Science

    (1995)
  • T Elbert et al.

    Input-increase and input-decrease types of cortical reorganization after upper extremity amputation in humans

    Exp Brain Res

    (1997)
  • S.L Florence et al.

    Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys

    J Neurosci

    (1995)
  • A.J Fuglevand et al.

    Short-term immobilization has a minimal effect on the strength and fatigability of a human hand muscle

    J Appl Physiol

    (1995)
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