Reducing the Uncertainty: Gating of Peripheral Inputs by Zona Incerta

Abstract

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.

Different Topography of the Reticulothalmic Inputs to First- and Higher-Order Somatosensory Thalamic Relays Revealed Using Photostimulation

“…This pattern could be explained by considerable variation in a single class of posterior nucleus neuron or by variations of experimental conditions, such as the extent of axons cut in the slices. On the other hand, this might suggest that there are multiple classes of these thalamic neurons related to different patterns of reticulothalamic input, which is consistent with the proposal that the posterior nucleus consists of distinct functional populations (Trageser and Keller 2004). In any case, our data are insufficient to distinguish between these possibilities of multiple classes or considerable variation within a single class.…”

A New Thalamic Pathway of Vibrissal Information Modulated by the Motor Cortex

“…As recently demonstrated, cortical inactivation only suppresses long-latency responses (ϳ15-20 ms) that are mediated by cortical feedback in intact animals (Lavallée et al, 2005). Shorter-latency vibrissal responses (ϳ8 ms), which persist after cortical lesion, only occur after lesion of the zona incerta, which exerts a strong feedforward inhibitory action in Po [Trageser and Keller, 2004;Lavallée et al (2005), their Discussion].…”

Noradrenergic Activation Amplifies Bottom-Up and Top-Down Signal-to-Noise Ratios in Sensory Thalamus

“…This indicates that the effects of the drugs are confined to a 1 mm area around the probe. This spread includes the VPM and nRt but may also affect parts of adjacent structures, such as the posterior nucleus and the zona incerta, both of which respond to whisker stimulation (Bartho et al, 2002;Trageser and Keller, 2004). Although potential effects mediated by these structures should be considered, we believe that these higher-order nuclei would be unlikely to explain most effects reported in the present paper.…”