Two dynamically distinct circuits drive inhibition in the sensory thalamus

Academic Article

Abstract

  • © 2020, The Author(s), under exclusive licence to Springer Nature Limited. Most sensory information destined for the neocortex is relayed through the thalamus, where considerable transformation occurs1,2. One means of transformation involves interactions between excitatory thalamocortical neurons that carry data to the cortex and inhibitory neurons of the thalamic reticular nucleus (TRN) that regulate the flow of those data3–6. Although the importance of the TRN has long been recognised7–9, understanding of its cell types, their organization and their functional properties has lagged behind that of the thalamocortical systems they control. Here we address this by investigating the somatosensory and visual circuits of the TRN in mice. In the somatosensory TRN we observed two groups of genetically defined neurons that are topographically segregated and physiologically distinct, and that connect reciprocally with independent thalamocortical nuclei through dynamically divergent synapses. Calbindin-expressing cells—located in the central core—connect with the ventral posterior nucleus, the primary somatosensory thalamocortical relay. By contrast, somatostatin-expressing cells—which reside along the surrounding edges of the TRN—synapse with the posterior medial thalamic nucleus, a higher-order structure that carries both top-down and bottom-up information10–12. The two TRN cell groups process their inputs in pathway-specific ways. Synapses from the ventral posterior nucleus to central TRN cells transmit rapid excitatory currents that depress deeply during repetitive activity, driving phasic spike output. Synapses from the posterior medial thalamic nucleus to edge TRN cells evoke slower, less depressing excitatory currents that drive more persistent spiking. Differences in the intrinsic physiology of TRN cell types, including state-dependent bursting, contribute to these output dynamics. The processing specializations of these two somatosensory TRN subcircuits therefore appear to be tuned to the signals they carry—a primary central subcircuit tuned to discrete sensory events, and a higher-order edge subcircuit tuned to temporally distributed signals integrated from multiple sources. The structure and function of visual TRN subcircuits closely resemble those of the somatosensory TRN. These results provide insights into how subnetworks of TRN neurons may differentially process distinct classes of thalamic information.
  • Published In

  • Nature  Journal
  • Digital Object Identifier (doi)

    Author List

  • Martinez-Garcia RI; Voelcker B; Zaltsman JB; Patrick SL; Stevens TR; Connors BW; Cruikshank SJ
  • Start Page

  • 813
  • End Page

  • 818
  • Volume

  • 583
  • Issue

  • 7818