State-Dependent Architecture of Thalamic Reticular Subnetworks

Abstract

Behavioral state is known to influence interactions between thalamus and cortex, which are important for sensation, action and cognition. The thalamic reticular nucleus (TRN) is hypothesized to regulate thalamo-cortical transmission, but the underlying functional architecture of this process and its state-dependence are unknown. By combining the first TRN ensemble recording with psychophysics and connectivity-based optogenetic tagging, we find that the TRN is composed of distinct sub-networks. While activity of limbic-projecting TRN neurons correlates with arousal, sensory-projecting neurons participate in spindles and show elevated synchrony by slow waves during sleep. Conversely, sensory-projecting neurons are suppressed by attentional states, demonstrating common microcircuit mechanisms of sensory processing in sleep and attention. Bidirectional manipulation of attentional performance was achieved through optogenetic manipulation of these TRN sub-networks. Our findings provide evidence for differential regulation of thalamic inhibition across brain states, suggesting that the TRN separately controls external stimulus processing and internally-generated computations, a basic determinant of cognitive function.

Thalamo-cortical communication, glutamatergic neurotransmission and neural oscillations: A unique window into the origins of ScZ?

“…Optogenetic approaches combined with multielectrode recordings support the idea that distinct subgroups of TRN neurons can facilitate the switching of attention from external stimuli (e.g. visual) to an internal one (Halassa et al, 2014).…”

“…Morever, TRN lesions induce disturbance of cortical delta and gamma oscillations and loss of sleep spindles (Marini et al, 2000;Steriade et al, 1985). Conversely, optogenetic activation of TRN rapidly leads to increased power of cortical delta oscillations (Lewis et al, 2015) and induction of cortical spindle-like discharges (Halassa et al, 2014;Halassa et al, 2011).…”

The thalamic reticular nucleus: A functional hub for thalamocortical network dysfunction in schizophrenia and a target for drug discovery

“…Furthermore, using recordings from microelectrode arrays in behaving mice, the same group discovered functional diversity amongst TRN microcircuits. Two TRN subpopulations were discovered, one that correlated with spindles and the other that correlated with arousal (Halassa et al, 2014) Cognition and behaviour…”

Intelligence neurocircuitry: cortical and subcortical structures

“…In the posterior fossa syndrome (one type of cerebellar cognitive-affective syndrome) that occurs 48 hours after the excision of a cerebellar tumor, children show mutism, buccolingual apraxia, apathy and poor spontaneous movements. Emotional lability is evident with distraction, irritability and agitation (Figure 3) (SCHMAHMANN and PANDYA, 2008;PINAULT, 2004;HALASSA, CHEN, WIMMER et al, 2014;STOODLEY and SCHMAHMANN, 2010;VOOGD, 2003;CAHANA-AMITAY and ALBERT, 2014).…”

“…They are important to the learning process, inducing focus and attention in the correct moment to allow learning; b) Thalamic intralaminar nucleus: responsible for the brainstem afferent specially for the nociception tracts and the ascending activator reticular system; c) Limbic nuclei: they are composed of ventral dorsal and medial nuclei, they participate in learning and memory, as well as motivation and personal experience; d) Thalamic specific nuclei: lateral and medial geniculate body, responsible, respectively for vision and hearing; e) Effector thalamic nuclei: receive afferent from pallidum and communicate with premotor areas, supplemental motor areas and posterior parietal lobe. They are related to motor functions and verbal fluency; f) Thalamic association nuclei: they connect with cortical areas of association, and they are related to complex cognitive functions (Figulre 2) (DUNCAN, 2013;PINAULT, 2004;HALASSA, CHEN, WIMMER et al, 2014).…”