Somatosensory control of thalamic relay neurons is regulated by two distinct layer 6 feedback systems

The medial posterior (POm) and ventral posterior medial (VPM) thalamic nuclei sort and filter somatosensory information that is sent to the primary somatosensory cortex (S1). Corticothalamic feedback from distinct cell populations of S1 layer 6 (S1L6) targets both POm and VPM. To differentiate their roles, electrophysiological recordings were conducted in awake mice during the photoinactivation of S1L6B-Drd1-expressing neurons (that project to POm), or S1L6-Ntsr1-expressing neurons (that project to POm and VPM). Photoinactivation of either pathway suppressed POm activity when whiskers were deflected, regardless of whisking state, but S1L6-Ntsr1-POm inputs were most affected when whisker deflection occurred during non-whisking. Conversely, S1L6-Ntsr1-VPM inputs responded to whisker deflections during whisking. We identified a novel projection from S1L6-Drd1-expressing neurons to the zona incerta, indicating a role for this GABAergic structure in a corticothalamic circuit that modulates POm. These results indicate corticothalamic control of somatosensory thalamus is regulated, in a context-dependent manner, by two distinct S1L6 feedback systems supporting precision and fine-tuning of somatosensory perception.