Alterations of motor cortical inhibition in patients with dystonia
Sabine Rona
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorCorresponding Author
Dr. Alfredo Berardelli
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Dipartimento di Scienze Neurologiche, Viale Università 30, 00185 Rome, ItalySearch for more papers by this authorLaura Vacca
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorMaurizio Inghilleri
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorMario Manfredi
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorSabine Rona
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorCorresponding Author
Dr. Alfredo Berardelli
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Dipartimento di Scienze Neurologiche, Viale Università 30, 00185 Rome, ItalySearch for more papers by this authorLaura Vacca
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorMaurizio Inghilleri
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorMario Manfredi
Department of Neurological Sciences, University of Rome “La Sapienza,” Rome, Italy; and Mediterranean Neurologic Institute Neuromed, Pozzilli (IS), Italy
Search for more papers by this authorAbstract
Cortical inhibitory mechanisms were investgated with the technique of paired transcranial magnetic stimulation in 10 patients with dystonia of the right arm: six patients had focal, task-specific dystonia (writer's cramp) and three had segmental and one had generalized dystonia. Paired stimuli were delivered in a conditioning-test design during slight voluntary activation of the target muscle, with subthreshold conditioning stimuli at short intervals (3-20 ms) and suprathreshold conditioning stimuli at long intervals (100-250 ms). The amount of inhibition at short interstimulus intervals did not differ significantly between patients and normal subjects. With long interstimulus intervals, patients showed more inhibition of the test response, which was significant at the 150-ms interval. The cortical silent period following a single suprathreshold magnetic stimulus was slightly shorter in patients. No significant difference was detected between the affected side and the unafected side in patients with unilateral task-specific dystonia, neither in the duration of the silent period nor in the respnse to paired magnetic stimuli. These results indicate that the different types of motor cortical inhibition are produced by different inhibitory circuits. We propose that the alterations observed in patients with dystonia are the result of impaired feedback from the basal ganglia to motor cortical areas, with the ultimate effect of a flattening of the excitability curve of the cortical motoneuron pool during voluntary muscle activation.
References
- 1 Marsden CD, Obeso JA, Zarranz JJ, Lang AE. The anatomical basis of symptomatic hemidystonia. Brain 1985; 108: 463–483.
- 2 Bhatia KP, Marsden CD. The behavioral and motor consequences of focal lesions of the basal ganglia in man. Brain 1994; 117: 859–876.
- 3 Lee MS, Marsden CD. Movement disorders following lesions of the thalamus or subthalamic region. Mov Disord 1994; 9: 493–507.
- 4 Karbe H, Holthoff VA, Rudolf J, Herholz K, Heiss WD. Positron emission tomography demonstrates frontal cortex and basal ganglia hypometabolism in dystonia. Neurology 1992; 42: 1540–1544.
- 5 Tempel LW, Perlmutter JS. Abnormal cortical responses in patients with writer's cramp. Neurology 1993; 43: 2252–2257.
- 6 Eidelberg D, Moeller JR, Ishikawa T, et al. The metabolic topography of idiopathic torsion dystonia. Brain 1995; 118: 1473–1484.
- 7 Ceballos-Baumann AO, Passingham RE, Warner T, Playford ED, Marsden CD, Brooks DJ. Overactive prefrontal and underactive motor cortical areas in idiopathic dystonia. Ann Neurol 1995; 37: 363–372.
- 8 Fève A, Bathien N, Rondot P. Abnormal movement related potentials in patients with lesions of the basal ganglia and anterior thalamus. J Neurol Neurosurg Psychiatry 1994; 57: 100–104.
- 9 Van Der Kamp W, Rothwell JC, Thompson PD, Day BL, Marsden CD. The movement-related cortical potential is abnormal in patients with idiopathic torsion dystonia. Mov Disord 1995; 10: 630–633.
- 10 Cantello R, Gianelli M, Bettucci D, Civardi C. Parkinson's disease rigidity: magnetic motor evoked potentials in a small hand muscle. Neurology 1991; 41: 1449–1456.
- 11 Valls-Solé J, Pascual-Leone A, Brasil-Neto JP, Cammarota A, Mc-Shane L, Hallett M. Abnormal facilitation of the response to transcranial magnetic stimulation in patients with Parkinson's disease. Neurology 1994; 44: 735–741.
- 12 Priori A, Berardelli A, Inghilleri M, Accornero N, Manfredi M. Motor cortical inhibition and the dopaminergic system. Brain 1994; 117: 317–323.
- 13 Priori A, Berardelli A, Inghilleri M, Polidori L, Manfredi M. Electromyographic silent period after transcranial brain stimulation in Huntington's disease. Mov Disord 1994; 9: 178–182.
- 14 Ridding MC, Inzelberg R, Rothwell JC. Changes in excitability of motor cortical circuitry in patients with Parkinson's disease. Ann Neurol 1995; 37: 181–188.
- 15 Berardelli A, Rona S, Inghilleri M, Manfredi M. Cortical inhibition in Parkinson's disease: a study with paired magnetic stimulation. Brain 1996; 119: 71–77.
- 16 Ikoma K, Samii A, Mercuri B, Wassermann EM, Hallett M. Abnormal cortical motor excitability in dystonia. Neurology 1996; 46: 1371–1376.
- 17 Ridding MC, Sheean G, Rothwell JC, Inzelberg R, Kujirai T. Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J Neurol Neurosurg Psychiatry 1995; 59: 493–498.
- 18 Kujirai T, Caramia MD, Rothwell JC, et al. Corticocortical inhibition in the human motor cortex. J Physiol (Lond) 1993; 471: 501–519.
- 19 Ridding MC, Taylor JL, Rothwell JC. The effect of voluntary contraction on corticocortical inhibition in human motor cortex. J Physiol (Lond) 1995; 487: 541–548.
- 20 Inghilleri M, Berardelli A, Cruccu G, Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervico-medullary junction. J Physiol (Lond) 1993; 466: 521–534.
- 21 Schell GR, Strick PL. The origin of thalamus inputs to the arcuate premotor and supplementary motor areas. J Neurosci 1984; 4: 539–560.
- 22 Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 1990; 13: 266–271. Comment in Trends Neurosci 1991; 14: 55–59.
- 23 Claus D, Weis M, Jahnke U, Plewe A, Brunhoelzl C. Corticospinal conduction studied with magnetic double stimulation in the intact human. J Neurol Sci 1992; 14: 180–188.
- 24 Valls-Solé J, Pascual-Leone A, Wassermann EM, Hallett M. Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol 1992; 85: 355–364.
- 25 Inghilleri M, Berardelli A, Cruccu G, Priori A, Manfredi M. Motor potentials evoked by paired cortical stimuli. Electroencephalorg Clin Neurophysiol 1990; 77: 382–389.
- 26 Fuhr P, Agostino R, Hallett M. Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 1991; 81: 257–262.
- 27 Wilson SA, Lockwood RJ, Thickbroom GW, Mastaglia FL. The muscle silent period following transcranial magnetic cortical stimulation. J Neurol Sci 1993; 114: 216–222.
- 28 Roick H, Von Giesen HJ, Benecke R. On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp Brain Res 1993; 94: 489–498.
- 29 Panizza ME, Hallett M, Nilsson J. Reciprocal inhibition in patients with hand cramps. Neurology 1989; 39: 85–89.
- 30 Nakashima K, Rothwell JC, Day BL, Thompson PD, Shannon K, Marsden CD. Reciprocal inhibition between forearm muscles in patients with writer's cramp and other occupational cramps, symptomatic hemidystonia and hemiparesis due to stroke. Brain 1989; 112: 681–697.
- 31 Deuschl G, Seifert C, Heinen F, Illert M, Lucking CH. Reciprocal inhibition of forearm flexor muscles in spasmodic torticollis. J Neurol Sci 1992; 113: 85–90.
- 32 Priori A, Berardelli A, Mercuri B, Manfredi M. Physiological effects produced by botulinum toxin treatment of upper limb dystonia: changes in reciprocal inhibition between forearm muscles. Brain 1995; 118: 801–807.
- 33 Panizza M, Lelli S, Nilsson J, Hallett M. H-reflex recovery curve and reciprocal inhibition of H-reflex in different kinds of dystonia. Neurology 1990; 40: 824–828.
- 34 Berardelli A, Rothwell JC, Day BL, Marsden CD. Pathophysiology of blepharospasm and oromandibular dystonia. Brain 1985; 108: 593–608.
- 35 Tolosa E, Montserrat L, Bayes A. Blink reflex studies in focal dystonias: enhanced excitability of brainstem interneurons in cranial dystonia and spasmodic torticollis. Mov Disord 1988; 3: 61–69.
- 36 Nakashima K, Rothwell JC, Thompson PD, et al. The blink reflex in patients with idiopathic torsion dystonia. Arch Neurol 1990; 47: 413–416.
- 37 Pauletti G, Berardelli A, Cruccu G, Agostino R, Manfredi M. Blink reflex and the masseter inhibitory reflex in patients with dystonia. Mov Disord 1993; 8: 495–500.
- 38 DeLong MR. Primate models of movement disorders of basal ganglia orgin. Trends Neurosci 1990; 13: 281–285.
- 39 Berardelli A, Accornero N, Argenta M, Meco G, Manfredi M. Fast complex arm movements in Parkinson's disease. J Neurol Neurosurg Psychiatry 1986; 49: 1146–1149.
- 40 Thompson PD, Berardelli A, Rothwell JC, et al. The coexistence of bradykinesia and chorea in Huntington's disease and its implications for theories of basal ganglia control of movement. Brain 1988; 111: 223–244.
- 41 Van Der Kamp W, Berardelli A, Rothwell JC, Thompson PD, Day BL, Marsden CD. Rapid elbow movements in patients with torsion dystonia. J Neurol Neurosurg Psychiatry 1989; 52: 1043–1049.
- 42 Agostino R, Berardelli A, Formica A, Accornero N, Manfredi M. Sequential arm movements in patients with Parkinson's disease, Huntington's disease and dystonia. Brain 1992; 115: 1481–1495.
- 43 Rona S, Vacca L, Manfredi GW, Inghilleri M, Berardelli A. Motor cortical excitability in patients with movement disorders [Abstract]. J Neurol 1995; 242(suppl): S63.
