Temporally coordinated activity among motor cortex, thalamus, and thalamic reticular nucleus neurons during rat forelimb movements

Thalamic reticular nucleus (TRN) neurons receive excitatory inputs from both cortical and thalamic neurons, and, in turn, inhibit thalamic relay neurons, thereby modulating thalamocortical signaling. Recent studies suggested that the TRN in the motor system contributes to precise temporal control within the cortico-thalamo-cortical loop. However, few studies have examined how TRN neurons temporally coordinate with cortical and thalamic neurons during discrete limb movements. Here, we investigated how TRN neurons collaborate with other neurons during forelimb movements depending on task demands. We trained head-fixed rats (male and female) to perform a lever-pull task using the forelimb at one of two difficulty levels (low- or high-demand task group). Spike activity was recorded from TRN neurons, some identified optogenetically, and from neurons in the primary motor cortex and ventral thalamus during task performance. Among these neurons, putative excitatory cortical neurons had the highest proportion of tonic spike activity before lever pull (Hold-type) and the lowest proportion of phasic pull-related activity (Pull-type), with the highest directional specificity. In contrast, TRN neurons exhibited more frequent Pull-type activity with lower directional specificity. Furthermore, rats in the high-demand group adopted a more uniform and robust strategy compared to those in the low-demand group. Notably, TRN neurons showed the greatest adaptive-like activity differences in association with task demands among those neurons: proportion of Pull-type neurons was higher, and their activity was greater, earlier, and more direction-specific. These results suggest that TRN neurons in the cortico-thalamo-cortical loop play a crucial role in dynamically controlling movements by adapting to circumstances.Significance statement The thalamic reticular nucleus (TRN), a key component of the cortico-thalamo-cortical loop, is thought to be critical for motor information processing. However, it remains unclear how this activity contributes to skilled limb movements when task demands change. We found that when the motor task was highly demanding, a population of TRN neurons showed adaptive-like activity differences. These neurons exhibited stronger, faster, and more directionally specific responses during movement execution. Our findings suggest that the TRN may act as a pivotal hub for optimizing the cortico-thalamo-cortical loop, enabling the adaptive motor control required for skilled movements.