Task-specific hand dystonia: can too much plasticity be bad for you?

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Patients with occupational hand dystonias have task-specific involuntary co-contraction and overflow of activity to inappropriate muscles. This interferes with highly skilled movements such as handwriting (writer's cramp) or playing a musical instrument (musician's cramp). Transcranial stimulation methods that probe mechanisms of synaptic plasticity in the motor cortex show an abnormal modifiability of sensorimotor circuits in patients with writer's cramp, probably because homeostatic control of the range of modification is deficient. We argue that during skilled motor practice, this leads to an excessive tendency to form associations between sensory inputs and motor outputs (abnormal potentiation) and to a failure to weaken already existing associations (deficient depotentiation). Deficient homeostatic control might be an important mechanism that triggers maladaptive reorganization and produces symptoms of occupational hand dystonias.

Introduction

Plasticity refers to the ability of the nervous system to change the effectiveness of transmission in neural circuits. This can involve changes in membrane properties such as a reduction in the threshold for initiation of an action potential, or changes in the effectiveness of synaptic transmission. Although much of the work on mechanisms of plasticity has been carried out in reduced animal preparations, several non-invasive neurophysiological methods have recently been developed that enable study of plasticity at a regional level in the human brain. The majority of these have focussed on the cerebral cortex and make use of techniques involving transcranial magnetic stimulation (TMS) or transcranial direct-current stimulation (TDCS).

Neural plasticity itself is almost always regarded as a ‘useful’ phenomenon that is important in learning and memory and could potentially compensate for dysfunction after injury. The question we address here is whether pathologies of the nervous system can result in abnormal plasticity and lead to identifiable clinical states. The model we propose is focal dystonia, in which patients have involuntary muscle contractions at rest or during the performance of intended movements 1, 2, 3. We argue that normal mechanisms of neural plasticity that are recruited after injury or during practice are subtly abnormal in some individuals. This leads to inappropriate associations between sensory input and motor output and the appearance of a characteristic movement disorder.

Section snippets

Clinical features and physiology of focal occupational dystonias

Dystonia can be defined as a syndrome characterized by prolonged muscle contractions that cause involuntary repetitive twisting movements and abnormal postures of the affected body parts [1]. The dystonic pattern can involve many segments of the entire body (generalized dystonia), one side of the body (hemidystonia), adjacent parts of the body (segmental dystonia) or a single body part in isolation (focal dystonia). In some focal dystonias, symptoms become apparent only if patients perform a

An animal model of aberrant plasticity leading to dystonia

In an influential study, Byl et al. [10] showed that monkeys who were over-trained to make a particular highly specific hand movement sometimes developed difficulties in moving their hands that appear similar to the problems of patients with focal hand dystonia. The somatosensory cortex of these animals was less well organized than that of healthy monkeys, with larger receptive fields and overlapping representations of the individual digits. A change in the pattern of connectivity in the

Transcranial stimulation techniques to study motor cortex plasticity in humans

TMS and TDCS are methods to stimulate the cerebral cortex painlessly through the intact skull and can be used to evoke plastic changes in the motor cortex. TMS was first introduced as a method to investigate the integrity of the corticospinal outflow from cerebral motor cortex to the spinal cord [12]. The TMS pulses readily penetrate the skull and carry an electric stimulating current into the cortex near the surface. In the motor area, this leads to activation of pyramidal neurons, conduction

Enhanced sensorimotor plasticity

These methods of investigating neural plasticity have enabled us to test the hypothesis that patients with dystonia have abnormal neural plasticity in the sensory and/or motor areas of cortex. In an early study, Siebner et al. [18] applied 1800 TMS pulses at 1 Hz over the premotor area of cortex and examined the after-effect on patterns of regional neuronal activity as indexed by PET measures of regional cerebral blood flow. Premotor rTMS led to a reduction in regional neuronal activity for at

Impaired homeostatic plasticity

What drives the abnormal responsiveness of the sensorimotor cortex in focal dystonia? As pointed out by many authors, the processes of neural plasticity have to be carefully controlled [30]. Plasticity that is too easy to induce might lead to formation of unwanted associations, whereas plasticity that is too difficult to produce leads to problems in learning anything new. This is apparent if we consider increasing the excitability of neural connections that have LTP-like behaviour [31]. The

Implications for current concepts of the pathophysiology of focal dystonia

Many physiological studies in patients with dystonia have indicated that there is reduced excitability of inhibitory mechanisms in spinal cord, brainstem and cortex [36]. This is complemented by imaging studies that show lower than normal GABA levels in the sensorimotor area of patients with hand dystonia [37]. Reduced inhibition in the sensorimotor system would lead to failure to suppress unintended movements of nearby muscles when a focal movement is being performed [38]. Our hypothesis does

Implications for current treatments of focal dystonia

Recognition that focal dystonias might be associated with disordered control of neural plasticity might also have implications for development of new therapeutic approaches to treatment. Some of these therapies have employed sensory training, on the basis that this might help patients to activate their muscles more selectively. Several others assume that the basic mechanisms of motor learning are intact and try to retrain movements through intensive practice 42, 43. Recently, it has been

Implications and conclusions

It should be noted that we do not assume that all forms of focal dystonia will show exactly the same patterns of abnormal plasticity. This is because there is good evidence that patient subgroups have differences in other physiological parameters that have been measured. For example, most idiopathic cases of focal dystonia have a mildly reduced sensory discrimination on the fingertips whereas cases of DYT1 dystonia do not [45]. Similarly, the motor cortex of patients with writer's cramp is less

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      Citation Excerpt :

      This task specificity likely results: from excessive practice in the presence of uncontrolled plasticity in the parieto-premotor pathway specialized in writing (Horovitz et al., 2013), thus leading to abnormal reorganization of the sensorimotor cortex and producing the classic dystonic posture. Occupational dystonia may develop only in predisposed individuals where subtle abnormalities of plasticity and other environmental factors, in combination with repetitive training, may induce the development of dystonic postures (Quartarone et al., 2006a,b). The role of repetitive training or other environmental factors is perhaps less important in generalized dystonia where more profound plasticity abnormalities may take place.

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