Clinical Neurophysiology 125 (2014) 655–656
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
How task specific is task specific dystonia? See Article, pages 786–797
Task specific dystonia is characterized by abnormal activation patterns of antagonist muscles during a specific manual task. The dystonic pattern may later ‘‘generalize’’ to other fine motor skills with the progression of the disease (Hallett, 2006). In simple writer’s cramp handwriting is impaired, but other tasks are not, whereas in complex writer’s cramp, dystonia may be activated by other manual skills such as shaving or makeup. In musician’s dystonia the task specificity is characterized by dystonic movements occurring only when playing a specific instrument. For instance a pianist may have difficulties in playing the piano, but may still perform well with the violin. Certain dystonic postures of the fingers or wrist may be relatively characteristic for the instrument provoking musician’s dystonia (Conti et al., 2008). Despite the fact, that task specific dystonias are often associated with excessive and repetitive performance of the certain skills, it remains enigmatic why the motor control deficit should be restricted to a single task. Previous kinematic studies found a less specific impairment of motor control in patients suffering from writer’s cramp with grip force abnormalities against the surface of a writing pen (Nowak et al., 2005), but also using the precision grip in a drawer opening task (Serrien et al., 2000). However, elevated grip force produced against a pen was not correlated with increased writing pressure (Hermsdorfer et al., 2011). In this issue of Clinical Neurophysiology, Schneider et al. used a very elegant design to address experimentally the relationship between grip force and dynamic force abnormalities during handwriting (Schneider et al., 2014). They asked writer’s cramp patients to perform three different tasks: in a first task the force exerted to the pen during writing was measured and compared to controls as previously described (Hermsdorfer et al., 2011). In a second task, subjects lifted, with the precision grip, a handle that was fixed to a box containing two different weights. The handle included a force sensor to measure the force exerted by the fingers. In a third task individuals moved a manipulandum along a vertical line up and down with increasing frequencies. A force sensor measured grip force and acceleration in three spatial dimensions. Controls showed correlations in grip force levels between the different tasks, while patients did not exhibit such correlations. In other words, the abnormally elevated grip force during handwriting could only be demonstrated for that specific task in writer’s cramp, while grip force levels in all other tasks were normal. Interestingly, this pattern was identical in patients with simple writer’s cramp and the twelve patients with complex writer’s cramp, whose dystonic co-contractions were clinically evident not only during writing, but also in other fine motor tasks.
This work is an important contribution to the current discussion, about the significance of task specificity and complexity in this type of dystonia, but contrasts to previous studies and the authors’ own expectations. Grip force control was found to be impaired in several previous studies with smaller patient numbers (Odergren et al., 1996; Prodoehl et al., 2006; Serrien et al., 2000). For precise motor control, afferent input is crucial and depends on feedback of tactile information (Westling and Johansson, 1984). For the initiation and the scaling of the grip response, tactile input seems to be essential (Macefield et al., 1996). Patients with writer’s cramp have difficulties in interpreting sensory input before or after a movement (Murase et al., 2000). Hence, one hypothesis on the pathophysiology of task specific dystonia postulates an impaired integration of sensory information into motor programming (Odergren et al., 1996). The results of Schneider and colleagues challenge this view, because the task specific grip force abnormality is not compatible with a general deficit of sensorimotor integration. Moreover, the authors suggest that the grip force applied depends on expectations and pre – learned motor strategies and may thus be voluntarily controlled. Therefore, increased force during writing in these patients could as well be regarded as a consequence and not the cause of writer’s cramp. Possibly, increased grip force during writing reflects the patients‘ attempt to compensate their deficit while performing that specific task in a very individual way rather than showing a primary deficit in sensorimotor control. However, previous findings of abnormal cortical excitability, abnormal sensory perception or a genetic predisposition point indeed towards a problem on a more global level of sensorimotor control, which should be reflected on a behavioral level (Hallett, 2006; Schmidt et al., 2011). A second concept to explain task specificity is the importance of fine tuning at low force levels in the skills typically affected by dystonia. The force exerted on a pen, a key or a string when playing an instrument is minimal. Hence, the most prominent common feature is an impairment of a high precision movement at low force exertion. Impaired surround inhibition in patients with task specific dystonia has been postulated, and recent studies demonstrated that surround inhibition is particularly disturbed in the generation of fine finger movements with low-force levels (Beck et al., 2009). Therefore one explanation of the task specificity in writer’s cramp patients could be decreased surround inhibition at low force levels during writing. A third notion that has been put forward is the influence of task complexity on intracortical inhibition (Beck and Hallett, 2010) in task specific dystonia. Writing or playing musical instruments
1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinph.2013.10.007
656
Editorial / Clinical Neurophysiology 125 (2014) 655–656
are extremely complex tasks compared to lifting a box or moving a manipulandum as applied by Schneider et al. Writing involves several different finger movements. A concept, which has been suggested, is that intracortical inhibition needs to be increased in the area that surrounds the cortical representation of muscles that are involved in a particular task such as writing or playing a musical instrument. These mechanisms seem to be important to individualize finger movement as required in those fine precision tasks (Sohn and Hallett, 2004a,b). Apparently, surround inhibition is stronger and occurs earlier in more complex tasks (Beck and Hallett, 2010). Complex tasks seem to be crucial to further clarify the pathophysiology of task specific dystonia. The results of the study of Schneider et al. demonstrated that grip force in task specific dystonia is normal in relatively simple control conditions such as lifting a handle or moving a manipulandum. Future studies should include analyzing grip force in other more complex tasks with a combination of different movement directions in patients with writer’s cramp and musician’s dystonia. Such more complex tasks could then possibly also serve as a model to evaluate other pathophysiological approaches. References Beck S, Hallett M. Surround inhibition is modulated by task difficulty. Clin Neurophysiol 2010;121:98–103. Beck S, Schubert M, Richardson SP, Hallett M. Surround inhibition depends on the force exerted and is abnormal in focal hand dystonia. J Appl Physiol 2009;107:1513–8. Conti AM, Pullman S, Frucht SJ. The hand that has forgotten its cunning–lessons from musicians’ hand dystonia. Mov Disord 2008;23:1398–406. Hallett M. Pathophysiology of writer’s cramp. Hum Mov Sci 2006;25:454–63. Hermsdorfer J, Marquardt C, Schneider AS, Furholzer W, Baur B. Significance of finger forces and kinematics during handwriting in writer’s cramp. Hum Mov Sci 2011;30:807–17. Macefield VG, Hager-Ross C, Johansson RS. Control of grip force during restraint of an object held between finger and thumb: responses of cutaneous afferents from the digits. Exp Brain Res 1996;108:155–71.
Murase N, Kaji R, Shimazu H, Katayama-Hirota M, Ikeda A, Kohara N, et al. Abnormal premovement gating of somatosensory input in writer’s cramp. Brain 2000;123:1813–29. Nowak DA, Rosenkranz K, Topka H, Rothwell J. Disturbances of grip force behaviour in focal hand dystonia: evidence for a generalised impairment of sensory-motor integration? J Neurol Neurosurg Psychiatry 2005;76:953–9. Odergren T, Iwasaki N, Borg J, Forssberg H. Impaired sensory-motor integration during grasping in writer’s cramp. Brain 1996;119:569–83. Prodoehl J, MacKinnon CD, Comella CL, Corcos DM. Rate of force production and relaxation is impaired in patients with focal hand dystonia. Parkinsonism Relat Disord 2006;12:363–71. Schmidt A, Jabusch HC, Altenmuller E, Enders L, Saunders-Pullman R, Bressman SB, et al. Phenotypic spectrum of musician’s dystonia: a task-specific disorder? Mov Disord 2011;26:546–9. Schneider AS, Fürholzer W, Marquardt C, Hermsdörfer J. Task specific grip force control in writer’s cramp. Clin Neurophysiol 2014;125:786–97. Serrien DJ, Burgunder JM, Wiesendanger M. Disturbed sensorimotor processing during control of precision grip in patients with writer’s cramp. Mov Disord 2000;15:965–72. Sohn YH, Hallett M. Disturbed surround inhibition in focal hand dystonia. Ann Neurol 2004a;56:595–9. Sohn YH, Hallett M. Surround inhibition in human motor system. Exp Brain Res 2004b;158:397–404. Westling G, Johansson RS. Factors influencing the force control during precision grip. Exp Brain Res 1984;53:277–84.
⇑
K.E. Zeuner Department of Neurology, Christian-Albrechts-University Kiel, Germany ⇑ Department of Neurology, Christian-Albrechts-University Kiel, University-Hospital Schleswig Holstein, Campus Kiel, Germany. Tel.: +49 431 597 8501; fax: +49 431 597 8502. E-mail address: [email protected] J. Volkmann Department of Neurology, University of Würzburg, Germany Available online 5 November 2013
Contents lists available at ScienceDirect
Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph
Editorial
How task specific is task specific dystonia? See Article, pages 786–797
Task specific dystonia is characterized by abnormal activation patterns of antagonist muscles during a specific manual task. The dystonic pattern may later ‘‘generalize’’ to other fine motor skills with the progression of the disease (Hallett, 2006). In simple writer’s cramp handwriting is impaired, but other tasks are not, whereas in complex writer’s cramp, dystonia may be activated by other manual skills such as shaving or makeup. In musician’s dystonia the task specificity is characterized by dystonic movements occurring only when playing a specific instrument. For instance a pianist may have difficulties in playing the piano, but may still perform well with the violin. Certain dystonic postures of the fingers or wrist may be relatively characteristic for the instrument provoking musician’s dystonia (Conti et al., 2008). Despite the fact, that task specific dystonias are often associated with excessive and repetitive performance of the certain skills, it remains enigmatic why the motor control deficit should be restricted to a single task. Previous kinematic studies found a less specific impairment of motor control in patients suffering from writer’s cramp with grip force abnormalities against the surface of a writing pen (Nowak et al., 2005), but also using the precision grip in a drawer opening task (Serrien et al., 2000). However, elevated grip force produced against a pen was not correlated with increased writing pressure (Hermsdorfer et al., 2011). In this issue of Clinical Neurophysiology, Schneider et al. used a very elegant design to address experimentally the relationship between grip force and dynamic force abnormalities during handwriting (Schneider et al., 2014). They asked writer’s cramp patients to perform three different tasks: in a first task the force exerted to the pen during writing was measured and compared to controls as previously described (Hermsdorfer et al., 2011). In a second task, subjects lifted, with the precision grip, a handle that was fixed to a box containing two different weights. The handle included a force sensor to measure the force exerted by the fingers. In a third task individuals moved a manipulandum along a vertical line up and down with increasing frequencies. A force sensor measured grip force and acceleration in three spatial dimensions. Controls showed correlations in grip force levels between the different tasks, while patients did not exhibit such correlations. In other words, the abnormally elevated grip force during handwriting could only be demonstrated for that specific task in writer’s cramp, while grip force levels in all other tasks were normal. Interestingly, this pattern was identical in patients with simple writer’s cramp and the twelve patients with complex writer’s cramp, whose dystonic co-contractions were clinically evident not only during writing, but also in other fine motor tasks.
This work is an important contribution to the current discussion, about the significance of task specificity and complexity in this type of dystonia, but contrasts to previous studies and the authors’ own expectations. Grip force control was found to be impaired in several previous studies with smaller patient numbers (Odergren et al., 1996; Prodoehl et al., 2006; Serrien et al., 2000). For precise motor control, afferent input is crucial and depends on feedback of tactile information (Westling and Johansson, 1984). For the initiation and the scaling of the grip response, tactile input seems to be essential (Macefield et al., 1996). Patients with writer’s cramp have difficulties in interpreting sensory input before or after a movement (Murase et al., 2000). Hence, one hypothesis on the pathophysiology of task specific dystonia postulates an impaired integration of sensory information into motor programming (Odergren et al., 1996). The results of Schneider and colleagues challenge this view, because the task specific grip force abnormality is not compatible with a general deficit of sensorimotor integration. Moreover, the authors suggest that the grip force applied depends on expectations and pre – learned motor strategies and may thus be voluntarily controlled. Therefore, increased force during writing in these patients could as well be regarded as a consequence and not the cause of writer’s cramp. Possibly, increased grip force during writing reflects the patients‘ attempt to compensate their deficit while performing that specific task in a very individual way rather than showing a primary deficit in sensorimotor control. However, previous findings of abnormal cortical excitability, abnormal sensory perception or a genetic predisposition point indeed towards a problem on a more global level of sensorimotor control, which should be reflected on a behavioral level (Hallett, 2006; Schmidt et al., 2011). A second concept to explain task specificity is the importance of fine tuning at low force levels in the skills typically affected by dystonia. The force exerted on a pen, a key or a string when playing an instrument is minimal. Hence, the most prominent common feature is an impairment of a high precision movement at low force exertion. Impaired surround inhibition in patients with task specific dystonia has been postulated, and recent studies demonstrated that surround inhibition is particularly disturbed in the generation of fine finger movements with low-force levels (Beck et al., 2009). Therefore one explanation of the task specificity in writer’s cramp patients could be decreased surround inhibition at low force levels during writing. A third notion that has been put forward is the influence of task complexity on intracortical inhibition (Beck and Hallett, 2010) in task specific dystonia. Writing or playing musical instruments
1388-2457/$36.00 Ó 2013 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinph.2013.10.007
656
Editorial / Clinical Neurophysiology 125 (2014) 655–656
are extremely complex tasks compared to lifting a box or moving a manipulandum as applied by Schneider et al. Writing involves several different finger movements. A concept, which has been suggested, is that intracortical inhibition needs to be increased in the area that surrounds the cortical representation of muscles that are involved in a particular task such as writing or playing a musical instrument. These mechanisms seem to be important to individualize finger movement as required in those fine precision tasks (Sohn and Hallett, 2004a,b). Apparently, surround inhibition is stronger and occurs earlier in more complex tasks (Beck and Hallett, 2010). Complex tasks seem to be crucial to further clarify the pathophysiology of task specific dystonia. The results of the study of Schneider et al. demonstrated that grip force in task specific dystonia is normal in relatively simple control conditions such as lifting a handle or moving a manipulandum. Future studies should include analyzing grip force in other more complex tasks with a combination of different movement directions in patients with writer’s cramp and musician’s dystonia. Such more complex tasks could then possibly also serve as a model to evaluate other pathophysiological approaches. References Beck S, Hallett M. Surround inhibition is modulated by task difficulty. Clin Neurophysiol 2010;121:98–103. Beck S, Schubert M, Richardson SP, Hallett M. Surround inhibition depends on the force exerted and is abnormal in focal hand dystonia. J Appl Physiol 2009;107:1513–8. Conti AM, Pullman S, Frucht SJ. The hand that has forgotten its cunning–lessons from musicians’ hand dystonia. Mov Disord 2008;23:1398–406. Hallett M. Pathophysiology of writer’s cramp. Hum Mov Sci 2006;25:454–63. Hermsdorfer J, Marquardt C, Schneider AS, Furholzer W, Baur B. Significance of finger forces and kinematics during handwriting in writer’s cramp. Hum Mov Sci 2011;30:807–17. Macefield VG, Hager-Ross C, Johansson RS. Control of grip force during restraint of an object held between finger and thumb: responses of cutaneous afferents from the digits. Exp Brain Res 1996;108:155–71.
Murase N, Kaji R, Shimazu H, Katayama-Hirota M, Ikeda A, Kohara N, et al. Abnormal premovement gating of somatosensory input in writer’s cramp. Brain 2000;123:1813–29. Nowak DA, Rosenkranz K, Topka H, Rothwell J. Disturbances of grip force behaviour in focal hand dystonia: evidence for a generalised impairment of sensory-motor integration? J Neurol Neurosurg Psychiatry 2005;76:953–9. Odergren T, Iwasaki N, Borg J, Forssberg H. Impaired sensory-motor integration during grasping in writer’s cramp. Brain 1996;119:569–83. Prodoehl J, MacKinnon CD, Comella CL, Corcos DM. Rate of force production and relaxation is impaired in patients with focal hand dystonia. Parkinsonism Relat Disord 2006;12:363–71. Schmidt A, Jabusch HC, Altenmuller E, Enders L, Saunders-Pullman R, Bressman SB, et al. Phenotypic spectrum of musician’s dystonia: a task-specific disorder? Mov Disord 2011;26:546–9. Schneider AS, Fürholzer W, Marquardt C, Hermsdörfer J. Task specific grip force control in writer’s cramp. Clin Neurophysiol 2014;125:786–97. Serrien DJ, Burgunder JM, Wiesendanger M. Disturbed sensorimotor processing during control of precision grip in patients with writer’s cramp. Mov Disord 2000;15:965–72. Sohn YH, Hallett M. Disturbed surround inhibition in focal hand dystonia. Ann Neurol 2004a;56:595–9. Sohn YH, Hallett M. Surround inhibition in human motor system. Exp Brain Res 2004b;158:397–404. Westling G, Johansson RS. Factors influencing the force control during precision grip. Exp Brain Res 1984;53:277–84.
⇑
K.E. Zeuner Department of Neurology, Christian-Albrechts-University Kiel, Germany ⇑ Department of Neurology, Christian-Albrechts-University Kiel, University-Hospital Schleswig Holstein, Campus Kiel, Germany. Tel.: +49 431 597 8501; fax: +49 431 597 8502. E-mail address: [email protected] J. Volkmann Department of Neurology, University of Würzburg, Germany Available online 5 November 2013
