Effects of optogenetic suppression of cortical input on primate thalamic neuronal activity during goal-directed behavior.

The motor thalamus relays signals from subcortical structures to the motor cortical areas. Previous studies in songbirds and rodents suggest that cortical feedback inputs crucially contribute to the generation of movement-related activity in the motor thalamus. In primates, however, it remains uncertain whether the corticothalamic projections may play a role in shaping neuronal activity in the motor thalamus. Here, using an optogenetic inactivation technique with the viral vector system expressing halorhodopsin, we investigated the role of cortical input in modulating thalamic neuronal activity during goal-directed behavior. In particular, we assessed whether suppression of signals originating from the supplementary eye field at the corticothalamic terminals could change the task-related neuronal modulation in the oculomotor thalamus in monkeys performing a self-initiated saccade task. We found that many thalamic neurons exhibited changes in their firing rates depending on saccade direction or task event, indicating that optical stimulation exerted task-specific effects on neuronal activity beyond the global changes in baseline activity. These results suggest that the corticothalamic projections might be actively involved in signal processing necessary for goal-directed behavior. However, we also found that some thalamic neurons exhibited overall, non-task-specific changes in the firing rate during optical stimulation, even in control animals without vector injections. The stimulation effects in these animals started with longer latency, implying a possible thermal effect on neuronal activity. Thus, our results not only reveal the importance of direct cortical input in neuronal activity in the primate motor thalamus, but also provide useful information for future optogenetic studies. Significance statement Although previous studies in songbirds and rodents have shown that corticothalamic inputs are essential for generating movement-related activity in the motor thalamus, their role in primates remains largely unknown. Here, we attempted to optogenetically suppress the corticothalamic terminals during neuronal recording from theoculomotor thalamus in monkeys performing a saccade task. We found that optical stimulation resulted in task-specific changes in the firing rate, indicating that thecorticothalamic projections are engaged in neural computations for goal-directed behavior. We also observed non-task-specific changes in baseline activity that mightbe caused by local heating of surrounding tissue, which underscores the importance of control experiments in animals without opsin expression.