State-Dependent Architecture of Thalamic Reticular Subnetworks

• Published in: Cell 2014-08, Vol.158 (4), p.808-821
• Main Authors: Halassa, Michael M., Chen, Zhe, Wimmer, Ralf D., Brunetti, Philip M., Zhao, Shengli, Zikopoulos, Basilis, Wang, Fan, Brown, Emery N., Wilson, Matthew A.
• Format: Article
• Language: English
• Subjects: Animals; Attention; Behavior, Animal; Cognition; Limbic System - physiology; Male; Mice; Mice, Inbred C57BL; Thalamic Nuclei - physiology; Visual Perception
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2014.06.025

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 interactions, 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 found reticular circuits to be composed of distinct subnetworks. While activity of limbic-projecting TRN neurons positively correlates with arousal, sensory-projecting neurons participate in spindles and show elevated synchrony by slow waves during sleep. Sensory-projecting neurons are suppressed by attentional states, demonstrating that their gating of thalamo-cortical interactions is matched to behavioral state. Bidirectional manipulation of attentional performance was achieved through subnetwork-specific optogenetic stimulation. Together, our findings provide evidence for differential inhibition of thalamic nuclei across brain states, where the TRN separately controls external sensory and internal limbic processing facilitating normal cognitive function. [Display omitted] [Display omitted] •Connectivity-based optogenetic TRN dissection reveals a subnetwork architecture•Sensory-projecting TRN regulates sensory processing across sleep and attention•Limbic-projecting TRN shows general regulation by arousal•Optogenetic suppression of visual-projecting TRN in attention enhances performance Distinct subnetworks in the thalamus reticular nucleus form a common circuit that regulates the communication between the thalamus and brain cortex during sleep and attentional states.