Task-related activity in the ventral thalamus, a major target of basal ganglia output, is often assumed to be permitted or triggered by changes in basal ganglia activity through gating- or rebound-like mechanisms. To test those hypotheses, we sampled single-unit activity from connected basal ganglia output and thalamic nuclei (globus pallidus-internus [GPi] and ventrolateral anterior nucleus [VLa]) in monkeys performing a reaching task. Rate increases were the most common peri-movement change in both nuclei. Moreover, peri-movement changes generally began earlier in VLa than in GPi. Simultaneously recorded GPi-VLa pairs rarely showed short-time-scale spike-to-spike correlations or slow across-trials covariations, and both were equally positive and negative. Finally, spontaneous GPi bursts and pauses were both followed by small, slow reductions in VLa rate. These results appear incompatible with standard gating and rebound models. Still, gating or rebound may be possible in other physiological situations: simulations show how GPi-VLa communication can scale with GPi synchrony and GPi-to-VLa convergence, illuminating how synchrony of basal ganglia output during motor learning or in pathological conditions may render this pathway effective. Thus, in the healthy state, basal ganglia-thalamic communication during learned movement is more subtle than expected, with changes in firing rates possibly being dominated by a common external source.
wordsRunning title: Basal ganglia-thalamic communication
AbstractTask-related activity in the ventral thalamus, a major target of basal ganglia (BG) output, is often assumed to be permitted or triggered by changes in BG activity through gating-or rebound-like mechanisms. To test those hypotheses, we sampled single-unit activity from connected BGoutput and thalamic nuclei (globus pallidus-internus, GPi, and ventrolateral-anterior nucleus, VLa) in monkeys performing a reaching task. Rate increases were the most common perimovement change in both nuclei. Moreover, peri-movement changes generally began earlier in VLa than in GPi. Simultaneously-recorded GPi-VLa pairs rarely showed short-timescale spiketo-spike correlations or slow across-trials covariations and both were equally positive and negative. Spontaneous GPi bursts and pauses were both followed by small reductions in VLa rate. These results appear incompatible with standard gating and rebound models. Instead, simulations show how GPi-VLa communication can scale with GPi synchrony and GPi-to-VLa convergence, thereby explaining these otherwise-incongruent findings and illuminating potential links to BG pathophysiology. Bouju et al. 2014a;Bosch-Bouju et al. 2014b;Person & Perkel 2005] may produce rebound bursts of thalamic activity following a cessation of transiently elevated inhibition from the BG (e.g., following task-related increases in BG output activity) [Bosch-Bouju et al. 2014a, Kim et al. 2017]. Both of these theories predict a tight temporal control of thalamic task-related responses by changes in BG output; more specifically, the latency of task-related changes in BG output activity should lead by a short time interval the resulting responses in thalamus. The gating hypothesis, in addition, predicts an inverse relationship in the signs of task-related changes in BG and BG-recipient thalamus, with the incidence (i.e., relative frequency of occurrence) of task-related increases in BG output associated with a proportional incidence of decreases in activity in BG-recipient thalamus.
2007; Bosch-
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