State-Dependent Processing of Sensory Stimuli by Thalamic Reticular Neurons

Abstract

Inhibitory neurons of the thalamic reticular (RT) nucleus fire in two activity modes, burst and tonic, depending on an animal's behavioral state. In tonic mode, depolarized RT cells fire single action potentials continuously, whereas burst firing consists of grouped discharges separated by periods of quiescence. To determine how these firing modes affect sensory-evoked RT responses, single-unit responses to controlled whisker deflections were analyzed according to the burst versus tonic mode of spontaneous activity (SA) preceding the response. After burst mode activity (i.e., either quiescence or spontaneous bursts), responses exhibited a slow approximately 15 msec rise to peak firing rates followed by a approximately 35 msec decay. Interspike intervals within the response exhibited accelerando-decelerando patterns similar to those of spontaneous bursts. After tonic mode activity (i.e., single spikes), responses had a nearly instantaneous approximately 1.5 msec rise-to-peak followed by a approximately 40 msec decay, with large spike counts (5.2 spikes per stimulus) similar to those evoked in burst mode (6.2 spikes per stimulus). Interspike intervals were longer in tonic mode and exhibited a decelerando pattern. Initial evoked spikes, however, had shorter latencies and greater synchrony, contributing to the rapid onset of tonic population response. Shifts from quiescent (presumed burst mode) to tonic SA could be induced by either previous whisker deflections or iontophoretic application of NMDA; both manipulations effected appropriate shifts from burst to tonic response spike patterns. In awake animals, burst and tonic firing in RT, as in thalamocortical relay nuclei, may reflect sensory processing strategies appropriate for different behavioral and attentional states.

Distinct Electrical and Chemical Connectivity Maps in the Thalamic Reticular Nucleus: Potential Roles in Synchronization and Sensation

“…Accordingly, in nRt cells with evoked spikelets, depolarization of the postsynaptic cell resulted in spikelet responses that were delayed and less intense. In the example shown in Figure 2 B, at a holding potential of 0 mV, glutamate uncaging evokes a short-latency cluster of 12 spikelets with a high-frequency (up to 200 Hz) accelerando-decellerando firing pattern characteristic of rat nRt cell burst firing (Hartings et al, 2003a). Depolarization of this postsynaptic neuron by 14 mV resulted in a delayed firing response, with fewer (10) spikelets occurring over an extended period of time.…”

“…Located between thalamus and cortex, the inhibitory thalamic reticular nucleus (nRt) plays key roles mediating selective attention (Montero, 2000;McAlonan et al, 2006), shaping sensory fields (Lee et al, 1994;Desilets-Roy et al, 2002;Hartings et al, 2003a), and generating neuronal rhythmic activities within the thalamocortical network Steriade et al, 1997). Relevant to these functions, nRt features (Pinault, 2004) include intrinsic membrane properties of the neurons [slow T-channel-mediated burst firing (Huguenard and Prince, 1992)], topographically organized reciprocal synaptic interconnections with excitatory thalamocortical cells (Jones, 1975), and mutual interactions between nRt cells mediated by chemical and/or electrical synapses (Landisman et al, 2002;Shu and McCormick, 2002;Long et al, 2004).…”

Circuits for Multisensory Integration and Attentional Modulation Through the Prefrontal Cortex and the Thalamic Reticular Nucleus in Primates

“…The TRN contains at least two types of neurons that exhibit two activity modes, burst and tonic. Importantly, the type of activity depends on the animal's behavioral state / 45,74,112,119,157,159 /. Dual discharge modes have also been observed in thalamic relay neurons but they differ in duration and interval between spikes / 47,100 /.…”

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

“…To test this possibility, we recorded from nRt cells, which were identifiable by their typical long-lasting responses to sensory stimulation and long burst firing (Hartings et al, 2000(Hartings et al, , 2003Castro-Alamancos, 2004b). Interspike interval histograms and autocorrelations for an nRt cell are shown in supplemental Figure S3 (available at www.jneurosci.org as supplemental material).…”

“…nRt regulates signal-to-noise levels in thalamocortical cells nRt cells that are responsive to whisker stimulation fire spontaneously in two different modes, a continuous tonic mode and a burst mode (Hartings et al, 2003). Noradrenergic activation produces the continuous tonic firing mode, whereas cholinergic activation suppresses nRt cell firing.…”