Neural activity during a simple reaching task in macaques is counter to gating and rebound in basal ganglia-thalamic communication

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-timescale 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.

作为基底节输出的主要靶点，腹侧丘脑（ventral thalamus）的任务相关活动通常被认为可通过门控或反弹样机制，由基底节活动的变化所允许或触发。为验证上述假说，我们在执行伸手任务的猕猴中，从相连的基底节输出核团与丘脑核团——内侧苍白球（globus pallidus-internus, GPi）与腹前外侧核（ventrolateral-anterior nucleus, VLa）——记录了单单元活动。在两个核团中，放电频率升高均为运动前后最常见的活动变化。此外，运动前后的活动变化通常在腹前外侧核中出现的时间早于内侧苍白球。同时记录的GPi-VLa核团配对极少出现短时间尺度的峰电位-峰电位相关性，或跨试次的缓慢协变；且这类相关性与协变的正负分布均较为均衡。最后，内侧苍白球的自发性爆发与暂停活动之后，均伴随腹前外侧核放电频率出现小幅且缓慢的下降。上述结果与标准的门控及反弹模型似乎并不兼容。不过，门控或反弹机制在其他生理情境中仍有可能存在：模拟实验表明，GPi-VLa的通讯强度可随GPi的同步性以及GPi到VLa的会聚投射规模变化而调整，这阐明了运动学习过程中或病理状态下基底节输出的同步性，可如何使该通路发挥有效作用。因此，在健康状态下，习得性运动过程中的基底节-丘脑通讯比预想中更为微妙，放电频率的变化可能由共同的外部来源主导。