Thalamic single neuron activity in patients with dystonia: Dystonia- related activity and somatic sensory reorganization

Frederick Lenz, C. J. Jaeger, M. S. Seike, Y. C. Lin, S. G. Reich, M. R. DeLong, J. L. Vitek

Research output: Contribution to journalArticle

Abstract

Indirect evidence suggests that the thalamus contributes to abnormal movements occurring in patients with dystonia (dystonia patients). The present study tested the hypothesis that thalamic activity contributes to the dystonic movements that occur in such patients. During these movements, spectral analysis of electromyographic (EMG) signals in flexor and extensor muscles of the wrist and elbow exhibited peak EMG power in the lowest frequency band [0-0.78 Hz (mean: 0.39 Hz) dystonia frequency] for 60-85% of epochs studied during a pointing task. Normal controls showed low-frequency peaks for 2 (P <0.001) for cells in presumed Vop often for dystonia patients (81%) but never for control patients. The percentage of such cells in presumed Vim of dystonia patients (32%) was not significantly different from that of controls (31%). Many cells in presumed Vop exhibited dystonia frequency activity that was correlated with and phase-advanced on EMG activity during dystonia, suggesting that this activity was related to dystonia. Thalamic somatic sensory activity also differed between dystonia patients and controls. The percentage of cells responding to passive joint movement or to manipulation of subcutaneous structures (deep sensory cells) in presumed Vim was significantly greater in patients with dystonia than in control patients undergoing surgery for treatment of pain or tremor. Dystonia patients had a significantly higher proportion of deep sensory cells responding to movement of more than one joint (26%, 13/52) than did 'control' patients (8%, 4/49). Deep sensory cells in patients with dystonia were located in thalamic maps that demonstrated increased representations of parts of the body affected by dystonia. Thus dystonia patients showed increased receptive fields and an increased thalamic representation of dystonic body parts. The motor activity of an individual sensory cell was related to the sensory activity of that cell by identification of the muscle apparently involved in the cell's receptive field. Specifically, we defined the effector muscle as the muscle that, by contraction, produced the joint movement associated with a thalamic neuronal sensory discharge, when the examiner passively moved the joint. Spike X EMG correlation functions during dystonia indicated that thalamic cellular activity less often was related to EMG in effector muscles (52%) than in other muscles (86%). Thus there is a mismatch between the effector muscle for a thalamic cell and the muscles with EMG correlated with activity of that cell during dystonia. This mismatch may result from the reorganization of sensory maps and may contribute to the simultaneous activation of multiple muscles observed in dystonia. Microstimulation in presumed Vim in dystonia patients produced simultaneous contraction of multiple forearm muscles, similar to the simultaneous muscle contractions observed in dystonia. These observations are consistent with a model in which sensory input to Vim in dystonia is transmitted through altered sensory maps to activate multiple muscles in the periphery, producing the overflow of muscle activation that is characteristic of dystonia.

Original languageEnglish (US)
Pages (from-to)2372-2392
Number of pages21
JournalJournal of Neurophysiology
Volume82
Issue number5
StatePublished - 1999

Fingerprint

Dystonia
Neurons
Muscles
Joints
Muscle Contraction
Human Body
Muscle Cells

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Lenz, F., Jaeger, C. J., Seike, M. S., Lin, Y. C., Reich, S. G., DeLong, M. R., & Vitek, J. L. (1999). Thalamic single neuron activity in patients with dystonia: Dystonia- related activity and somatic sensory reorganization. Journal of Neurophysiology, 82(5), 2372-2392.

Thalamic single neuron activity in patients with dystonia : Dystonia- related activity and somatic sensory reorganization. / Lenz, Frederick; Jaeger, C. J.; Seike, M. S.; Lin, Y. C.; Reich, S. G.; DeLong, M. R.; Vitek, J. L.

In: Journal of Neurophysiology, Vol. 82, No. 5, 1999, p. 2372-2392.

Research output: Contribution to journalArticle

Lenz, F, Jaeger, CJ, Seike, MS, Lin, YC, Reich, SG, DeLong, MR & Vitek, JL 1999, 'Thalamic single neuron activity in patients with dystonia: Dystonia- related activity and somatic sensory reorganization', Journal of Neurophysiology, vol. 82, no. 5, pp. 2372-2392.
Lenz, Frederick ; Jaeger, C. J. ; Seike, M. S. ; Lin, Y. C. ; Reich, S. G. ; DeLong, M. R. ; Vitek, J. L. / Thalamic single neuron activity in patients with dystonia : Dystonia- related activity and somatic sensory reorganization. In: Journal of Neurophysiology. 1999 ; Vol. 82, No. 5. pp. 2372-2392.
@article{894c4636d4f545e6838a82903bbdb3f3,
title = "Thalamic single neuron activity in patients with dystonia: Dystonia- related activity and somatic sensory reorganization",
abstract = "Indirect evidence suggests that the thalamus contributes to abnormal movements occurring in patients with dystonia (dystonia patients). The present study tested the hypothesis that thalamic activity contributes to the dystonic movements that occur in such patients. During these movements, spectral analysis of electromyographic (EMG) signals in flexor and extensor muscles of the wrist and elbow exhibited peak EMG power in the lowest frequency band [0-0.78 Hz (mean: 0.39 Hz) dystonia frequency] for 60-85{\%} of epochs studied during a pointing task. Normal controls showed low-frequency peaks for 2 (P <0.001) for cells in presumed Vop often for dystonia patients (81{\%}) but never for control patients. The percentage of such cells in presumed Vim of dystonia patients (32{\%}) was not significantly different from that of controls (31{\%}). Many cells in presumed Vop exhibited dystonia frequency activity that was correlated with and phase-advanced on EMG activity during dystonia, suggesting that this activity was related to dystonia. Thalamic somatic sensory activity also differed between dystonia patients and controls. The percentage of cells responding to passive joint movement or to manipulation of subcutaneous structures (deep sensory cells) in presumed Vim was significantly greater in patients with dystonia than in control patients undergoing surgery for treatment of pain or tremor. Dystonia patients had a significantly higher proportion of deep sensory cells responding to movement of more than one joint (26{\%}, 13/52) than did 'control' patients (8{\%}, 4/49). Deep sensory cells in patients with dystonia were located in thalamic maps that demonstrated increased representations of parts of the body affected by dystonia. Thus dystonia patients showed increased receptive fields and an increased thalamic representation of dystonic body parts. The motor activity of an individual sensory cell was related to the sensory activity of that cell by identification of the muscle apparently involved in the cell's receptive field. Specifically, we defined the effector muscle as the muscle that, by contraction, produced the joint movement associated with a thalamic neuronal sensory discharge, when the examiner passively moved the joint. Spike X EMG correlation functions during dystonia indicated that thalamic cellular activity less often was related to EMG in effector muscles (52{\%}) than in other muscles (86{\%}). Thus there is a mismatch between the effector muscle for a thalamic cell and the muscles with EMG correlated with activity of that cell during dystonia. This mismatch may result from the reorganization of sensory maps and may contribute to the simultaneous activation of multiple muscles observed in dystonia. Microstimulation in presumed Vim in dystonia patients produced simultaneous contraction of multiple forearm muscles, similar to the simultaneous muscle contractions observed in dystonia. These observations are consistent with a model in which sensory input to Vim in dystonia is transmitted through altered sensory maps to activate multiple muscles in the periphery, producing the overflow of muscle activation that is characteristic of dystonia.",
author = "Frederick Lenz and Jaeger, {C. J.} and Seike, {M. S.} and Lin, {Y. C.} and Reich, {S. G.} and DeLong, {M. R.} and Vitek, {J. L.}",
year = "1999",
language = "English (US)",
volume = "82",
pages = "2372--2392",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "5",

}

TY - JOUR

T1 - Thalamic single neuron activity in patients with dystonia

T2 - Dystonia- related activity and somatic sensory reorganization

AU - Lenz, Frederick

AU - Jaeger, C. J.

AU - Seike, M. S.

AU - Lin, Y. C.

AU - Reich, S. G.

AU - DeLong, M. R.

AU - Vitek, J. L.

PY - 1999

Y1 - 1999

N2 - Indirect evidence suggests that the thalamus contributes to abnormal movements occurring in patients with dystonia (dystonia patients). The present study tested the hypothesis that thalamic activity contributes to the dystonic movements that occur in such patients. During these movements, spectral analysis of electromyographic (EMG) signals in flexor and extensor muscles of the wrist and elbow exhibited peak EMG power in the lowest frequency band [0-0.78 Hz (mean: 0.39 Hz) dystonia frequency] for 60-85% of epochs studied during a pointing task. Normal controls showed low-frequency peaks for 2 (P <0.001) for cells in presumed Vop often for dystonia patients (81%) but never for control patients. The percentage of such cells in presumed Vim of dystonia patients (32%) was not significantly different from that of controls (31%). Many cells in presumed Vop exhibited dystonia frequency activity that was correlated with and phase-advanced on EMG activity during dystonia, suggesting that this activity was related to dystonia. Thalamic somatic sensory activity also differed between dystonia patients and controls. The percentage of cells responding to passive joint movement or to manipulation of subcutaneous structures (deep sensory cells) in presumed Vim was significantly greater in patients with dystonia than in control patients undergoing surgery for treatment of pain or tremor. Dystonia patients had a significantly higher proportion of deep sensory cells responding to movement of more than one joint (26%, 13/52) than did 'control' patients (8%, 4/49). Deep sensory cells in patients with dystonia were located in thalamic maps that demonstrated increased representations of parts of the body affected by dystonia. Thus dystonia patients showed increased receptive fields and an increased thalamic representation of dystonic body parts. The motor activity of an individual sensory cell was related to the sensory activity of that cell by identification of the muscle apparently involved in the cell's receptive field. Specifically, we defined the effector muscle as the muscle that, by contraction, produced the joint movement associated with a thalamic neuronal sensory discharge, when the examiner passively moved the joint. Spike X EMG correlation functions during dystonia indicated that thalamic cellular activity less often was related to EMG in effector muscles (52%) than in other muscles (86%). Thus there is a mismatch between the effector muscle for a thalamic cell and the muscles with EMG correlated with activity of that cell during dystonia. This mismatch may result from the reorganization of sensory maps and may contribute to the simultaneous activation of multiple muscles observed in dystonia. Microstimulation in presumed Vim in dystonia patients produced simultaneous contraction of multiple forearm muscles, similar to the simultaneous muscle contractions observed in dystonia. These observations are consistent with a model in which sensory input to Vim in dystonia is transmitted through altered sensory maps to activate multiple muscles in the periphery, producing the overflow of muscle activation that is characteristic of dystonia.

AB - Indirect evidence suggests that the thalamus contributes to abnormal movements occurring in patients with dystonia (dystonia patients). The present study tested the hypothesis that thalamic activity contributes to the dystonic movements that occur in such patients. During these movements, spectral analysis of electromyographic (EMG) signals in flexor and extensor muscles of the wrist and elbow exhibited peak EMG power in the lowest frequency band [0-0.78 Hz (mean: 0.39 Hz) dystonia frequency] for 60-85% of epochs studied during a pointing task. Normal controls showed low-frequency peaks for 2 (P <0.001) for cells in presumed Vop often for dystonia patients (81%) but never for control patients. The percentage of such cells in presumed Vim of dystonia patients (32%) was not significantly different from that of controls (31%). Many cells in presumed Vop exhibited dystonia frequency activity that was correlated with and phase-advanced on EMG activity during dystonia, suggesting that this activity was related to dystonia. Thalamic somatic sensory activity also differed between dystonia patients and controls. The percentage of cells responding to passive joint movement or to manipulation of subcutaneous structures (deep sensory cells) in presumed Vim was significantly greater in patients with dystonia than in control patients undergoing surgery for treatment of pain or tremor. Dystonia patients had a significantly higher proportion of deep sensory cells responding to movement of more than one joint (26%, 13/52) than did 'control' patients (8%, 4/49). Deep sensory cells in patients with dystonia were located in thalamic maps that demonstrated increased representations of parts of the body affected by dystonia. Thus dystonia patients showed increased receptive fields and an increased thalamic representation of dystonic body parts. The motor activity of an individual sensory cell was related to the sensory activity of that cell by identification of the muscle apparently involved in the cell's receptive field. Specifically, we defined the effector muscle as the muscle that, by contraction, produced the joint movement associated with a thalamic neuronal sensory discharge, when the examiner passively moved the joint. Spike X EMG correlation functions during dystonia indicated that thalamic cellular activity less often was related to EMG in effector muscles (52%) than in other muscles (86%). Thus there is a mismatch between the effector muscle for a thalamic cell and the muscles with EMG correlated with activity of that cell during dystonia. This mismatch may result from the reorganization of sensory maps and may contribute to the simultaneous activation of multiple muscles observed in dystonia. Microstimulation in presumed Vim in dystonia patients produced simultaneous contraction of multiple forearm muscles, similar to the simultaneous muscle contractions observed in dystonia. These observations are consistent with a model in which sensory input to Vim in dystonia is transmitted through altered sensory maps to activate multiple muscles in the periphery, producing the overflow of muscle activation that is characteristic of dystonia.

UR - http://www.scopus.com/inward/record.url?scp=0032740182&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0032740182&partnerID=8YFLogxK

M3 - Article

C2 - 10561412

AN - SCOPUS:0032740182

VL - 82

SP - 2372

EP - 2392

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 5

ER -