NEUROLOGY 1996;47:508-520
© 1996 American Academy of Neurology
A primate genesis model of focal dystonia and repetitive strain injuryI. Learning-induced dedifferentiation of the representation of the hand in the primary somatosensory cortex in adult monkeys
Nancy N. Byl, PhD, PT,
Michael M. Merzenich, PhD and
William M. Jenkins, PhD
From the Coleman Laboratory and Keck Center for Integrative Neurosciences, Departments of Otolaryngology and Physiology, University of California at San Francisco, San Francisco, CA 94143-0732.
Received August 30, 1995. Accepted in final form August 30, 1995.
Address correspondence and reprint requests to Dr. Nancy N. Byl, Director, Graduate Program in Physical Therapy, University of California at San Francisco School of Medicine, 374 Parnassus Avenue, Room 301, San Francisco, CA 94143-0376.
In this study we tested a neuroplasticity/learning origins hypothesis for repetitive strain injuries (RSIs), including occupationally induced focal dystonia.Repetitive movements produced in a specific form and in an appropriate behavioral context cause a degradation of the sensory feedback information controlling fine motor movements, resulting in the ``learned'' genesis of RSIs. Two adult New World owl monkeys were trained at a behavioral task that required them to maintain an attended grasp on a hand grip that repetitively and rapidly (20 msec) opened and closed over short distances. The monkeys completed 300 behavioral trials per day (1,100 to 3,000 movement events) with an accuracy of 80 to 90%. A movement control disorder was recorded in both monkeys. Training was continued until the performance accuracy dropped to below 50%. We subsequently conducted an electrophysiologic mapping study of the representations of the hand within the primary somatosensory (SI) cortical zone. The hand representation in the true primary somatosensory cortical field, SI area 3b, was found to be markedly degraded in these monkeys, as characterized by (1) a dedifferentiation of cortical representations of the skin of the hand manifested by receptive fields that were 10 to 20 times larger than normal, (2) the emergence of many receptive fields that covered the entire glabrous surface of individual digits or that extended across the surfaces of two or more digits, (3) a breakdown of the normally sharply segregated area 3b representations of volar glabrous and dorsal hairy skin of the hand, and (4) a breakdown of the local shifted-overlap receptive field topography of area 3b, with many digital receptive fields overlapping the fields of neurons sampled in cortical penetrations up to more than four times farther apart than normal. Thus, rapid, repetitive, highly stereotypic movements applied in a learning context can actively degrade cortical representations of sensory information guiding fine motor hand movements. This cortical plasticity/learning-based dedifferentiation of sensory feedback information from the hand contributes to the genesis of occupationally derived repetitive strain injuries, including focal dystonia of the hand. Successful treatment of patients with RSI will plausibly require learning-based restoration of differentiated representations of sensory feedback information from the hand.
NEUROLOGY 1996;47: 508-520
This article has been cited by other articles:
|
|
|
|
 
A Scontrini, A Conte, G Defazio, M Fiorio, G Fabbrini, A Suppa, M Tinazzi, and A Berardelli
Somatosensory temporal discrimination in patients with primary focal dystonia
J. Neurol. Neurosurg. Psychiatry,
December 1, 2009;
80(12):
1315 - 1319.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Rosenkranz, K. Butler, A. Williamon, and J. C. Rothwell
Regaining Motor Control in Musician's Dystonia by Restoring Sensorimotor Organization
J. Neurosci.,
November 18, 2009;
29(46):
14627 - 14636.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. M. Schabrun, C. M. Stinear, W. D. Byblow, and M. C. Ridding
Normalizing Motor Cortex Representations in Focal Hand Dystonia
Cereb Cortex,
September 1, 2009;
19(9):
1968 - 1977.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. M. Barlow
The Communication Neuroscience Laboratories at the University of Kansas: An Overview
Speech Science and Orofacial Disorders,
July 1, 2009;
19(1):
18 - 27.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Tamura, Y. Ueki, P. Lin, S. Vorbach, T. Mima, R. Kakigi, and M. Hallett
Disordered plasticity in the primary somatosensory cortex in focal hand dystonia
Brain,
March 1, 2009;
132(3):
749 - 755.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Roze, A. Soumare, I. Pironneau, S. Sangla, V. C. de Cock, A. Teixeira, A. Astorquiza, C. Bonnet, J. P. Bleton, M. Vidailhet, et al.
Case-control study of writer's cramp
Brain,
March 1, 2009;
132(3):
756 - 764.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. D. Andreatta
Sensorimotor Elements of the Orofacial System: Reviewing the Basics
Speech Science and Orofacial Disorders,
October 1, 2008;
18(2):
51 - 61.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Tsao, M. P. Galea, and P. W. Hodges
Reorganization of the motor cortex is associated with postural control deficits in recurrent low back pain
Brain,
August 1, 2008;
131(8):
2161 - 2171.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. L. Ludlow, J. Hoit, R. Kent, L. O. Ramig, R. Shrivastav, E. Strand, K. Yorkston, and C. M. Sapienza
Translating Principles of Neural Plasticity Into Research on Speech Motor Control Recovery and Rehabilitation
J Speech Lang Hear Res,
February 1, 2008;
51(1):
S240 - S258.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Carbon, M. F. Ghilardi, M. Argyelan, V. Dhawan, S. B. Bressman, and D. Eidelberg
Increased cerebellar activation during sequence learning in DYT1 carriers: an equiperformance study
Brain,
January 1, 2008;
131(1):
146 - 154.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Dashtipour, M. Barahimi, and S. Karkar
Cervical Dystonia
Journal of Pharmacy Practice,
December 1, 2007;
20(6):
449 - 457.
[Abstract]
[PDF]
|
|
|
|
|
|
|
E. F. Chang, R. S. Turner, J. L. Ostrem, V. R. Davis, and P. A. Starr
Neuronal Responses to Passive Movement in the Globus Pallidus Internus in Primary Dystonia
J Neurophysiol,
December 1, 2007;
98(6):
3696 - 3707.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Defazio, A. Berardelli, and M. Hallett
Do primary adult-onset focal dystonias share aetiological factors?
Brain,
May 1, 2007;
130(5):
1183 - 1193.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. M. Smith, P. Lunga, D. Story, N. Harris, J. Le Belle, M. F James, J. D. Pickard, and J. W. Fawcett
Inosine promotes recovery of skilled motor function in a model of focal brain injury
Brain,
April 1, 2007;
130(4):
915 - 925.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. T Lin, E. A Shamim, and M. Hallett
Focal hand dystonia
Practical Neurology,
October 1, 2006;
6(5):
278 - 287.
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Peller, K. E. Zeuner, A. Munchau, A. Quartarone, M. Weiss, A. Knutzen, M. Hallett, G. Deuschl, and H. R. Siebner
The basal ganglia are hyperactive during the discrimination of tactile stimuli in writer's cramp
Brain,
October 1, 2006;
129(10):
2697 - 2708.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. W. Mahncke, B. B. Connor, J. Appelman, O. N. Ahsanuddin, J. L. Hardy, R. A. Wood, N. M. Joyce, T. Boniske, S. M. Atkins, and M. M. Merzenich
Memory enhancement in healthy older adults using a brain plasticity-based training program: A randomized, controlled study
PNAS,
August 15, 2006;
103(33):
12523 - 12528.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Quartarone, A. Sant'Angelo, F. Battaglia, S. Bagnato, V. Rizzo, F. Morgante, J. C. Rothwell, H. R. Siebner, and P. Girlanda
Enhanced Long-Term Potentiation-Like Plasticity of the Trigeminal Blink Reflex Circuit in Blepharospasm
J. Neurosci.,
January 11, 2006;
26(2):
716 - 721.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Dresel, B. Haslinger, F. Castrop, A. M. Wohlschlaeger, and A. O. Ceballos-Baumann
Silent event-related fMRI reveals deficient motor and enhanced somatosensory activation in orofacial dystonia
Brain,
January 1, 2006;
129(1):
36 - 46.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Haslinger, P. Erhard, C. Dresel, F. Castrop, M. Roettinger, and A. O. Ceballos-Baumann
"Silent event-related" fMRI reveals reduced sensorimotor activation in laryngeal dystonia
Neurology,
November 22, 2005;
65(10):
1562 - 1569.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Hesse, C. Werner, M. Pohl, S. Rueckriem, J. Mehrholz, and M.L. Lingnau
Computerized Arm Training Improves the Motor Control of the Severely Affected Arm After Stroke: A Single-Blinded Randomized Trial in Two Centers
Stroke,
September 1, 2005;
36(9):
1960 - 1966.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. A. Starr, G. M. Rau, V. Davis, W. J. Marks Jr., J. L. Ostrem, D. Simmons, N. Lindsey, and R. S. Turner
Spontaneous Pallidal Neuronal Activity in Human Dystonia: Comparison With Parkinson's Disease and Normal Macaque
J Neurophysiol,
June 1, 2005;
93(6):
3165 - 3176.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Delmaire, A. Krainik, S. Tezenas du Montcel, E. Gerardin, S. Meunier, J. -F. Mangin, S. Sangla, L. Garnero, M. Vidailhet, and S. Lehericy
Disorganized somatotopy in the putamen of patients with focal hand dystonia
Neurology,
April 26, 2005;
64(8):
1391 - 1396.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Rosenkranz, A. Williamon, K. Butler, C. Cordivari, A. J. Lees, and J. C. Rothwell
Pathophysiological differences between musician's dystonia and writer's cramp
Brain,
April 1, 2005;
128(4):
918 - 931.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. C. Mednick, A. C. Arman, and G. M. Boynton
The time course and specificity of perceptual deterioration
PNAS,
March 8, 2005;
102(10):
3881 - 3885.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Murase, J. C. Rothwell, R. Kaji, R. Urushihara, K. Nakamura, N. Murayama, T. Igasaki, M. Sakata-Igasaki, T. Mima, A. Ikeda, et al.
Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer's cramp
Brain,
January 1, 2005;
128(1):
104 - 115.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Rosenkranz and J. C Rothwell
The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex
J. Physiol.,
November 15, 2004;
561(1):
307 - 320.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Elbert and B. Rockstroh
Reorganization of Human Cerebral Cortex: The Range of Changes Following Use and Injury
Neuroscientist,
April 1, 2004;
10(2):
129 - 141.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. Ohara, N. Weiss, and F. A. Lenz
Microstimulation in the Region of the Human Thalamic Principal Somatic Sensory Nucleus Evokes Sensations Like Those of Mechanical Stimulation and Movement
J Neurophysiol,
February 1, 2004;
91(2):
736 - 745.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Classen
Focal hand dystonia - a disorder of neuroplasticity?
Brain,
December 1, 2003;
126(12):
2571 - 2572.
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Quartarone, S. Bagnato, V. Rizzo, H. R. Siebner, V. Dattola, A. Scalfari, F. Morgante, F. Battaglia, M. Romano, and P. Girlanda
Abnormal associative plasticity of the human motor cortex in writer's cramp
Brain,
December 1, 2003;
126(12):
2586 - 2596.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T D Sanger
Childhood onset generalised dystonia can be modelled by increased gain in the indirect basal ganglia pathway
J. Neurol. Neurosurg. Psychiatry,
November 1, 2003;
74(11):
1509 - 1515.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. M. Molloy, T. D. Carr, K. E. Zeuner, J. M. Dambrosia, and M. Hallett
Abnormalities of spatial discrimination in focal and generalized dystonia
Brain,
October 1, 2003;
126(10):
2175 - 2182.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Byl, J. Roderick, O. Mohamed, M. Hanny, J. Kotler, A. Smith, M. Tang, and G. Abrams
Effectiveness of Sensory and Motor Rehabilitation of the Upper Limb Following the Principles of Neuroplasticity: Patients Stable Poststroke
Neurorehabil Neural Repair,
September 1, 2003;
17(3):
176 - 191.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R. J. Nudo
Retuning the misfiring brain
PNAS,
June 24, 2003;
100(13):
7425 - 7427.
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Candia, C. Wienbruch, T. Elbert, B. Rockstroh, and W. Ray
Effective behavioral treatment of focal hand dystonia in musicians alters somatosensory cortical organization
PNAS,
June 24, 2003;
100(13):
7942 - 7946.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. H. Anca, Tcipora Falik Zaccai, S. Badarna, A. M. Lozano, A. E. Lang, and N. Giladi
Natural History of Oppenheim's Dystonia (DYT1) in Israel
J Child Neurol,
May 1, 2003;
18(5):
325 - 330.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. Meunier, S. Lehericy, L. Garnero, and M. Vidailhet
Dystonia: Lessons from Brain Mapping
Neuroscientist,
February 1, 2003;
9(1):
76 - 81.
[Abstract]
[PDF]
|
|
|
|
|
|
|
G. LUNDBORG, B. ROSEN, L. KNUTSSON, S. HOLTAS, F. STAHLBERG, and E. M. LARSSON
Hand-Arm-Vibration Syndrome (HAVS): Is There a Central Nervous Component? an fMRI Study
J Hand Surg Eur Vol.,
December 1, 2002;
27(6):
514 - 519.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. Tamburin, P. Manganotti, C. A. Marzi, A. Fiaschi, and G. Zanette
Abnormal somatotopic arrangement of sensorimotor interactions in dystonic patients
Brain,
December 1, 2002;
125(12):
2719 - 2730.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Sailer, G. F Molnar, D. I Cunic, and R. Chen
Effects of peripheral sensory input on cortical inhibition in humans
J. Physiol.,
October 15, 2002;
544(2):
617 - 629.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. T. Blake, F. Strata, A. K. Churchland, and M. M. Merzenich
Neural correlates of instrumental learning in primary auditory cortex
PNAS,
July 23, 2002;
99(15):
10114 - 10119.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Lehericy, S. Grand, P. Pollak, F. Poupon, J.-F. Le Bas, P. Limousin, P. Jedynak, C. Marsault, Y. Agid, and M. Vidailhet
Clinical characteristics and topography of lesions in movement disorders due to thalamic lesions
Neurology,
September 25, 2001;
57(6):
1055 - 1066.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Priori, A. Pesenti, A. Cappellari, G. Scarlato, and S. Barbieri
Limb immobilization for the treatment of focal occupational dystonia
Neurology,
August 14, 2001;
57(3):
405 - 409.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. P. Kilgard, P. K. Pandya, J. Vazquez, A. Gehi, C. E. Schreiner, and M. M. Merzenich
Sensory Input Directs Spatial and Temporal Plasticity in Primary Auditory Cortex
J Neurophysiol,
July 1, 2001;
86(1):
326 - 338.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. S. Kim
Delayed onset mixed involuntary movements after thalamic stroke: Clinical, radiological and pathophysiological findings
Brain,
February 1, 2001;
124(2):
299 - 309.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Munchau, S. Corna, M. A. Gresty, K. P. Bhatia, J. D. Palmer, D. Dressler, N. P. Quinn, J. C. Rothwell, and A. M. Bronstein
Abnormal interaction between vestibular and voluntary head control in patients with spasmodic torticollis
Brain,
January 1, 2001;
124(1):
47 - 59.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. Bara-Jimenez, P. Shelton;, and M. Hallett
Spatial discrimination is abnormal in focal hand dystonia
Neurology,
December 26, 2000;
55(12):
1869 - 1873.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. D. Sanger and M. M. Merzenich
Computational Model of the Role of Sensory Disorganization in Focal Task-Specific Dystonia
J Neurophysiol,
November 1, 2000;
84(5):
2458 - 2464.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Murase, R. Kaji, H. Shimazu, M. Katayama-Hirota, A. Ikeda, N. Kohara, J. Kimura, H. Shibasaki, and J. C. Rothwell
Abnormal premovement gating of somatosensory input in writer's cramp
Brain,
September 1, 2000;
123(9):
1813 - 1829.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. LUNDBORG
Brain Plasticity and Hand Surgery: an Overview
J Hand Surg Eur Vol.,
June 1, 2000;
25(3):
242 - 252.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M. Tinazzi, A. Priori, L. Bertolasi, E. Frasson, F. Mauguiere, and A. Fiaschi
Abnormal central integration of a dual somatosensory input in dystonia : Evidence for sensory overflow
Brain,
January 1, 2000;
123(1):
42 - 50.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. A. Lenz and N. N. Byl
Reorganization in the Cutaneous Core of the Human Thalamic Principal Somatic Sensory Nucleus (Ventral Caudal) in Patients With Dystonia
J Neurophysiol,
December 1, 1999;
82(6):
3204 - 3212.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. A. Lenz, C. J. Jaeger, M. S. Seike, Y. C. Lin, S. G. Reich, M. R. DeLong, and J. L. Vitek
Thalamic Single Neuron Activity in Patients With Dystonia: Dystonia-Related Activity and Somatic Sensory Reorganization
J Neurophysiol,
November 1, 1999;
82(5):
2372 - 2392.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Vidailhet, C. Dupel, S. Lehericy, P. Remy, D. Dormont, M. Serdaru, P. Jedynak, H. Veber, Y. Samson, C. Marsault, et al.
Dopaminergic Dysfunction in Midbrain Dystonia: Anatomoclinical Study Using 3-Dimensional Magnetic Resonance Imaging and Fluorodopa F 18 Positron Emission Tomography
Arch Neurol,
August 1, 1999;
56(8):
982 - 989.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Yazawa, A. Ikeda, R. Kaji, K. Terada, T. Nagamine, K.-i. Toma, T. Kubori, J. Kimura, and H. Shibasaki1
Abnormal cortical processing of voluntary muscle relaxation in patients with focal hand dystonia studied by movement-related potentials
Brain,
July 1, 1999;
122(7):
1357 - 1366.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. J. Feiwell, K. J. Black, L. A. McGee-Minnich, A. Z. Snyder, A.-M. MacLeod, and J. S. Perlmutter
Diminished regional cerebral blood flow response to vibration in patients with blepharospasm
Neurology,
January 1, 1999;
52(2):
291 - 291.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Sankhla, E. C Lai, and J. Jankovic
Peripherally induced oromandibular dystonia
J. Neurol. Neurosurg. Psychiatry,
November 1, 1998;
65(5):
722 - 728.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
J. L Janavs and M. J Aminoff
Dystonia and chorea in acquired systemic disorders
J. Neurol. Neurosurg. Psychiatry,
October 1, 1998;
65(4):
436 - 445.
[Full Text]
|
|
|
|
|
|
|
A. Sterr, M. M. Muller, T. Elbert, B. Rockstroh, C. Pantev, and E. Taub
Perceptual Correlates of Changes in Cortical Representation of Fingers in Blind Multifinger Braille Readers
J. Neurosci.,
June 1, 1998;
18(11):
4417 - 4423.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. J. Schicatano, M. A. Basso, and C. Evinger
Animal Model Explains the Origins of the Cranial Dystonia Benign Essential Blepharospasm
J Neurophysiol,
May 1, 1997;
77(5):
2842 - 2846.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
