The activity of primate ventrolateral thalamic neurones during motor adaptation.

Abstract

Three monkeys were trained to perform stereotyped wrist movements to track a target (phase 1). Changing the gain between the wrist movement and visual display required the monkey to adapt its wrist movement. This adaptation consisted of progressive reduction of movement amplitude over a number of trials (phase 2) until a stereotyped movement accommodating the new gain was learned (phase 3). The experiment's aim was to investigate whether cerebellar thalamic neuronal discharge (ND) changed during motor adaptation and whether this change was related to scaling of kinematic parameters or movement error. Extracellular single-cell recordings were made from "wrist-related" neurones in the cerebellar thalamus (59) and the nucleus ventro-posterior lateralis caudalis (VPLc) (37) of each monkey while they performed the movement paradigm. Neurones were selected for further analysis (37/59 cerebellar thalamic and 23/37 VPLc) if phase-1 movements were stereotyped and motor adaptation occurred in phase 2 (according to statistical definitions). When the gain initially changed, there were positional errors in the form of overshoot. Adaptation to the new gain was achieved by a variety of strategies, including modification of the amplitude of kinematic parameters and positional error in addition to reduction of time to peak velocity and movement time. During stereotyped movements, most cerebellar thalamic neurones fired before movement onset and before VPLc neurones. During adaptation, this order of onset of firing was reversed, and cerebellar thalamic neurones discharged after VPLc neurones and close to the onset of movement. During motor adaptation, the mean rate of phasic ND rose in a large proportion of cerebellar thalamic and VPLc neurones, and the proportion of cerebellar thalamic neurones that encoded a signal about positional error and movement amplitude also increased. In addition, there is set-related activity in the discharge of a majority of cerebellar thalamic and VPLc neurones. This does not appear to be specifically related to motor adaptation, but is related to the movement amplitude. We have discussed the role of the cerebello-thalamo-cortical pathway in error detection in the light of the similarities between discharge patterns of cerebellar thalamic and VPLc neurones. We speculate that, when learned movements are performed, the discharge of cerebellar thalamic neurones occurs before movement, perhaps representing an efference copy of the intended movement. During adaptation, this signal is gated out, and later-arriving peripheral afferent input dominates cerebellar thalamic discharge.