Regular articleTask-specific plasticity of somatosensory cortex in patients with writer's cramp
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).
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