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

Thalamic single neuron activity in patients with dystonia: dystonia-related activity and somatic sensory reorganization. J. Neurophysiol. 82: 2372-239 2, 1999. Indirect evidence suggests that the thalamus contributes to abnorm al movements occurring in patients with dystonia (dystonia patients). The p resent study tested the hypothesis that thalamic activity contributes to th e dystonic movements that occur in such patients. During these movements, s pectral analysis of electromyographic (EMG) signals in flexor and extensor muscles of the wrist and elbow exhibited peak EMG power in the lowest frequ ency band [0-0.78 Hz (mean: 0.39 Hz) dystonia frequency] for 60-85% of epoc hs studied during a pointing task. Normal controls showed low-frequency pea ks for <16% of epochs during pointing. Among dystonia patients, simultaneou s contraction of antagonistic muscles (cocontraction) at dystonia frequency during pointing was observed for muscles acting about the wrist (63% of ep ochs) and elbow (39%), but cocontraction was not observed among normal cont rols during pointing. Thalamic neuronal signals were recorded during thalam otomy for treatment of dystonia and were compared with those of control pat ients 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 anteri or border of the principal sensory nucleus (ventral caudal, Vc) with the re gion 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 nev er for control patients. The percentage of such cells in presumed Vim of dy stonia patients (32%) was not significantly different from that of controls (31%). Many cells in presumed Vop exhibited dystonia frequency activity th at was correlated with and phase-advanced on EMG activity during dystonia, suggesting that this activity was related to dystonia. Thalamic somatic sen sory activity also differed between dystonia patients and controls. The per centage of cells responding to passive joint movement or to manipulation of subcutaneous structures (deep sensory cells) in presumed Vim was significa ntly greater in patients with dystonia than in control patients undergoing surgery for treatment of pain or tremor. Dystonia patients had a significan tly 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 se nsory cells in patients with dystonia were located in thalamic maps that de monstrated increased representations of parts of the body affected by dysto nia. Thus dystonia patients showed increased receptive fields and an increa sed thalamic representation of dystonic body parts. The motor activity of a n 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 neuron al 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 ot her 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 co ntribute to the simultaneous activation of multiple muscles observed in dys tonia. Microstimulation in presumed Vim in dystonia patients produced simul taneous contraction of multiple forearm muscles, similar to the simultaneou s muscle contractions observed in dystonia. These observations are consiste nt with a model in which sensory input to Vim in dystonia is transmitted th rough altered sensory maps to activate multiple muscles in the periphery, p roducing the overflow of muscle activation that is characteristic of dyston ia.