Elsevier

NeuroImage

Volume 20, Issue 2, October 2003, Pages 1329-1338
NeuroImage

Regular article
Task-specific plasticity of somatosensory cortex in patients with writer's cramp

https://doi.org/10.1016/S1053-8119(03)00375-6Get rights and content

Abstract

Focal dystonias such as writer's cramp are characterized by muscular cramps that accompany the execution of specific motor tasks. Until now, the pathophysiology of focal dystonia remains incompletely understood. Recent studies suggest that the development of writer's cramp is related to abnormal organization of primary somatosensory cortex (SI), which in turn leads to impaired motor function. To explore contributions of SI on mechanisms of task specificity in focal dystonia, we investigated dynamic alterations in the functional organization of SI as well as sensory-motor gating for rest, left- and right-handed writing and brushing in writer's cramp patients and healthy controls. The functional organization of somatosensory cortex was assessed by neuromagnetic source imaging (151 channel whole-head MEG). In accordance with previous reports, distances between cortical representations of thumb and little finger of the affected hand were smaller in patients compared to healthy subjects. However, similar to healthy controls, patients showed normal modulation of the functional organization of SI as induced by the execution of different motor tasks. Both in the control subjects and patients, cortical distances between representations of thumb and little finger increased when writing and brushing compared to the resting condition. Although, cramps only occured during writing, no differences in the organization of SI were seen among motor tasks. Our data suggest that despite alterations in the organization of primary somatosensory cortex in writer's cramp, the capability of SI to adapt dynamically to different tasks is not impaired.

Introduction

Focal dystonias such as writer's cramp are characterized by involuntary muscle contractions that accompany the execution of motor tasks. One striking clinical feature of focal dystonias is that spasms of arm and hand muscles are frequently triggered by the execution of specific motor tasks or limb postures (Marsden and Sheehy, 1990). Although, dystonic cramping may be triggered by a variety of motor tasks and even at rest, in severe forms of focal dystonia context-specific initiation of dystonic muscle activation can be seen at all stages of the disease. In writer's cramp, as one type of focal dystonia, hand positions typical for writing induce spastic contractions of muscles in the hand. Writing with modified hand postures, or writing while simultaneously stimulating the hand—sometimes referred to as “geste antagonistique”—can prevent or reduce cramping (Gomez-Wong et al., 1998).

The pathophysiology of writer's cramp remains unclear (Lim et al., 2001). Abnormal processing within the basal ganglia Berardelli et al., 1998, Chen and Hallett, 1998, Hallett, 1998, Rona et al., 1998, Naumann et al., 2000, motor cortical areas Ikeda et al., 1996, Ikoma et al., 1996, Filipovic et al., 1997, Yazawa et al., 1999, Siebner et al., 1999, Toro et al., 2000, or within the premotor area or supplementary motor cortex Ibanez et al., 1999, Hamano et al., 1999, Curra et al., 2000, Oga et al., 2002 have been discussed as potential sources of focal dystonia. It has recently been suggested that a perturbed interaction between somatosensory and motor cortex could play a crucial role in the pathogenesis of focal dystonia Odergren et al., 1996, Byl et al., 1997, Chen and Hallett, 1998, Elbert et al., 1998, Hallett, 1998, Sanger and Merzenich, 2000, Bara-Jimenez et al., 2000. More specifically, it has been suggested that dedifferentiation and degradation of representational zones in primary somatosensory cortex represent the pathogenetic basis of focal dystonia (Byl et al., 1996). According to this hypothesis, the processing of reafferent sensory input important for movement control is impaired and motor cortex is not supplied with adequate sensory feedback. As a consequence, motor output may not be well adjusted causing cramps in target muscles (Sanger and Merzenich, 2000). Alterations in the functional organization of somatosensory cortex have been demonstrated in patients suffering from musician's cramp Elbert et al., 1998, Candia et al., 1999, Byl et al., 2000 as well as writer's cramp (Bara-Jimenez et al., 1998). In both groups of patients, reduced distances between individual finger representation in primary somatosensory cortex were demonstrated using neuroelectric and neuromagnetic source localization. These results were interpreted as largely overlapping, undifferentiated cortical finger representations associated with impaired sensorimotor integration.

Recent data suggest that somatosensory cortex is capable of rapidly changing its functional organization depending on task and context conditions in humans (Braun et al., 2000) and animals (Moore et al., 1999). For example, in healthy subjects individual cortical finger representations become more segregated during writing compared to rest (Braun et al., 2001). Therefore, it is conceivable that similarly rapid changes in the functional organization of somatosensory cortex that occur in a task-dependent manner could be involved in the pathogenesis of focal dystonia. In particular, if writer's cramp patients assume a hand posture typical for writing, context-dependent disorganization of primary somatosensory cortex might be induced, which in turn may trigger involuntary cramping.

To elucidate the role of primary somatosensory cortex in task-dependent occurrence of focal dystonia, sensory processing during different motor tasks including tasks that elicit cramps should be investigated. In the present experiment, dynamic changes in the functional organization of somatosensory cortex and its activation during rest, writing, and brushing were investigated in writer's cramp patients using neuromagnetic imaging. In particular, functional organization of SI and “sensory-motor gating,” the reduction of activation of SI during the performance of motor tasks, were examined. If changes within somatosensory cortex are involved in the pathogenesis of writer's cramp, it would be expected that physiological responses during writing would differ from brushing, a movement similar to writing that does not elicit cramps in patients. As unilateral focal dystonia is associated with abnormal organization of both hemispheres (Meunier et al., 2001), task-dependent changes in the processing of tactile stimuli were investigated for stimulation and movement execution of both the left and right hand. Patients' results were compared to a group of healthy controls.

Section snippets

Subjects

Seven right-handed patients (according to the Edinburgh Inventory of handedness; Oldfield, 1971), 5 males and 2 females between 33 and 67 years (mean ± SD; 46 ± 12 years) participated in the study. Data obtained in patients were compared to a group of 7 right-handed healthy subjects (female: 3, male: 4) of similar age (mean ± SD: 39 ± 9 years, range between 24 and 48 years). The experimental procedures were approved by the local ethics committee and all subjects gave informed consent after

Patients reports

Patients reported involuntary cramping of hand muscles only during right-hand writing. Three patients had to make several short breaks due to intolerable painful cramps. No cramping was observed during left-handed writing, rest, or brushing.

Electromyography

EMG activity was recorded to verify whether writing in patients induced increased muscular activity compared to brushing and resting, and compared to the muscular activity in control subjects. The EMG recording of one patient was lost due to technical

Discussion

In the present study neuromagnetic source imaging was applied to probe the functional organization of somatosensory cortex in writer's cramp patients and healthy subjects during different movement conditions and during rest. Three major results were obtained. (1) During rest focal dystonia patients revealed a reduced distance between the cortical representations of thumb and little finger on both hemispheres compared to healthy controls. (2) Similar to healthy subjects, a modified functional

Acknowledgements

We gratefully thank Mrs. Gabi Walker-Dietrich for skillful technical assistance during the experimental procedures. We also thank Dr. Ben Seymour for native speaker assistance in editing the manuscript. Furthermore, we owe many thanks to the reviewers for their constructive and helpful comments and suggestions. Research supported by Deutsche Forschungsgemeinschaft SFB 550 (projects B4 and C6). Participation of K.W. was supported by the Deutsche Forschungsgemeinschaft (Wi 1957/2-1).

References (53)

  • V.K. Lim et al.

    Focal dystoniacurrent theories

    Hum. Mov. Sci.

    (2001)
  • C.D. Marsden et al.

    Writer's cramp

    Trends Neurosci.

    (1990)
  • C.I. Moore et al.

    Dynamics of neural processing in rat somatosensory cortex

    Trends Neurosci.

    (1999)
  • R.C. Oldfield

    The assessment and analysis of handednessthe Edinburgh inventory

    Neuropsychologia

    (1971)
  • J. Pujol et al.

    Brain cortical activation during guitar-induced hand dystonia studied by functional MRI

    Neuroimage

    (2000)
  • P.M. Rossini et al.

    “Gating” of human short-latency somatosensory evoked cortical responses during execution of movement. A high resolution electroencephalography study

    Brain Res.

    (1999)
  • G. Abbruzzese et al.

    Proprioceptive modulation of somatosensory evoked potentials during active or passive finger movements in man

    J. Neurol. Neurosurg. Psychiatry

    (1981)
  • W. Bara-Jimenez et al.

    Abnormal somatosensory homunculus in dystonia of the hand

    Ann. Neurol.

    (1998)
  • W. Bara-Jimenez et al.

    Sensory discrimination capabilities in patients with focal hand dystonia

    Ann. Neurol.

    (2000)
  • A. Berardelli et al.

    The pathophysiology of primary dystonia

    Brain

    (1998)
  • N. Birbaumer et al.

    Effects of regional anesthesia on phantom limb pain are mirrored in changes in cortical reorganization

    J. Neurosci.

    (1997)
  • C. Braun et al.

    Dynamic organization of the somatosensory cortex induced by motor activity

    Brain

    (2001)
  • C. Braun et al.

    Diffential activation in somatosensory cortex for different discrimination tasks

    J. Neurosci.

    (2000)
  • R.E. Burke et al.

    Validity and reliability of a rating scale for the primary torsion dystonias

    Neurology

    (1985)
  • N.N. Byl et al.

    A primate model for studying focal dystonia and repetitive strain injuryeffects on the primary somatosensory cortex

    Phys. Ther.

    (1997)
  • N.N. Byl et al.

    A primate model of focal dystonia and repetitive strain injury. 1. Learning induced dedifferentiation of the representation of the hand in primary somatosensory cortex in adult monkeys

    Neurology

    (1996)
  • Cited by (39)

    • Pathophysiology of Dystonia

      2016, Handbook of Behavioral Neuroscience
      Citation Excerpt :

      Defects in spatial and temporal discrimination of sensory stimuli have been reported in patients with focal dystonia. Moreover, both symptomatic and nonmanifesting subjects of inherited forms of dystonia showed similar sensory abnormalities (Braun et al., 2003; Scontrini et al., 2009; Tinazzi et al., 2009). Another major theme in the pathophysiology of dystonia is abnormal plasticity of sensorimotor areas, which further unifies the above mentioned neurophysiological substrates of the disease.

    • Neuroanatomical correlates of dystonic tremor: A cross-sectional study

      2014, Parkinsonism and Related Disorders
      Citation Excerpt :

      Interestingly, the same neuroanatomical pattern has been described in patients affected by focal dystonia [15]. In fact, patients with cervical dystonia, blepharospasm or writer's cramp are characterized by an abnormal increase of volume in the sensorimotor cortex [15] together with abnormal activities of this cortical region as detected by functional MRI [16,17], as well as by a disordered cortical representation of digits as detected by magnetoencephalography technique [18]. All this evidence allow us to hypothesize that focal dystonia and DT might share some pathophysiological mechanisms characterized by impaired sensorimotor integration or abnormal sensorimotor somatotopy.

    • Cortical pattern of complex but not simple movements is affected in writer's cramp: A parametric event-related fMRI study

      2012, Clinical Neurophysiology
      Citation Excerpt :

      As expected, the greatest BOLD signal differences were found in the sensory part of the SM1 cortex and in the SII cortex in our WC patients. This is in agreement with theory of aberrant involvement of the receptive fields in the somatosensory cortex (Bara-Jimenez et al., 2000; Braun et al., 2003; Elbert et al., 1998; Fiorio et al., 2006; Meunier et al., 2001, Nelson et al., 2009), with the hypothesis of disordered sensorimotor integration at the cortical level (Abbruzzese et al., 2001; Roze et al., 2009; Vidailhet et al., 2009) and with the results of several functional imaging studies (Butterworth et al., 2003; Hu et al., 2006; Ibanez et al., 1999; Islam et al., 2009; Lerner et al., 2004; Odergren et al.,1998; Oga et al., 2002; Wu et al., 2010). As also confirmed by our previous study, the somatosensory cortex has an important role in the pathogenesis of dystonia since repeated transcranial magnetic stimulation of the S1 cortex proved to have an unambiguously positive effect on WC patients (Havránková et al., 2010).

    View all citing articles on Scopus
    View full text