Reducing the uncertainty: gating of peripheral inputs by zona incerta.

Sensory inputs are relayed to the neocortex by "first-order" thalamic nuclei, the responses of which are determined by ascending inputs from peripheral receptors. In contrast, "higher-order" thalamic nuclei respond poorly to peripheral inputs, and their responses are thought to be determined by descending cortical inputs. We tested this hypothesis by recording from neurons in the higher-order somatosensory posterior medial (POm) nucleus of narcotized rats. As reported previously, POm neurons responded to whisker stimuli with long-latency (median, 27 msec) and low-magnitude responses, consistent with cortically driven responses. However, when we suppressed inhibitory inputs from the subthalamic nucleus zona incerta (ZI), POm responses were of significantly higher magnitude and shorter latency, with many POm neurons responding at latencies consistent with ascending driving inputs from trigeminal nuclei. Our data suggest that POm comprises two neuronal populations: one population is driven by both peripheral and cortical inputs, and the second population responds only to cortical inputs. These findings demonstrate that ZI gates peripheral inputs to POm, enabling it to function both as a first-order and higher-order nucleus. Because ZI innervates all higher-order nuclei, this gating mechanism may exert similar regulation of thalamic processing in other sensory systems.