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The Journal of Neurophysiology Vol. 82 No. 5 November 1999, pp. 2372-2392
Copyright ©1999 by the American Physiological Society
Departments of 1Neurosurgery and 2Neurology, Johns Hopkins Hospital, Baltimore, Maryland, 21287-7713; and 3Department of Neurology, Emory University, Atlanta, Georgia 30322
Lenz, F. A.,
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. 82: 2372-2392, 1999. 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 <16% of epochs
during pointing. Among dystonia patients, simultaneous contraction of
antagonistic muscles (cocontraction) at dystonia frequency during
pointing was observed for muscles acting about the wrist (63% of
epochs) and elbow (39%), but cocontraction was not observed among
normal controls during pointing. Thalamic neuronal signals were
recorded during thalamotomy for treatment of dystonia and were compared
with those of control patients without motor abnormality who were
undergoing thalamic procedures for treatment of chronic pain. Presumed
nuclear boundaries of a human thalamic cerebellar relay nucleus
(ventral intermediate, Vim) and a pallidal relay nucleus (ventral oral
posterior, Vop) were estimated by aligning the anterior border of the
principal sensory nucleus (ventral caudal, Vc) with the region where
the majority of cells have cutaneous receptive fields (RFs). The ratio
of power at dystonia frequency to average spectral power was >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.
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