A Thalamic Reticular Circuit for Head Direction Cell Tuning and Spatial Navigation

• Published in: Cell reports (Cambridge) Vol. 31; no. 10; p. 107747
• Main Authors: Vantomme, Gil, Rovó, Zita, Cardis, Romain, Béard, Elidie, Katsioudi, Georgia, Guadagno, Angelo, Perrenoud, Virginie, Fernandez, Laura M.J., Lüthi, Anita
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 09-06-2020
• Subjects: allocentric; Animals; anterior thalamus; burst discharge; chemogenetics; egocentric; Head - physiology; Mice; optogenetics; perseverance; presubiculum; retrosplenial cortex; Spatial Navigation - physiology; synaptic inhibition; Thalamic Nuclei - physiology; synaptic inhibition; optogenetics; chemogenetics; burst discharge; perseverance; presubiculum; egocentric; allocentric; anterior thalamus; retrosplenial cortex
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2020.107747

As we navigate in space, external landmarks and internal information guide our movement. Circuit and synaptic mechanisms that integrate these cues with head-direction (HD) signals remain, however, unclear. We identify an excitatory synaptic projection from the presubiculum (PreS) and the multisensory-associative retrosplenial cortex (RSC) to the anterodorsal thalamic reticular nucleus (TRN), so far classically implied in gating sensory information flow. In vitro, projections to TRN involve AMPA/NMDA-type glutamate receptors that initiate TRN cell burst discharge and feedforward inhibition of anterior thalamic nuclei. In vivo, chemogenetic anterodorsal TRN inhibition modulates PreS/RSC-induced anterior thalamic firing dynamics, broadens the tuning of thalamic HD cells, and leads to preferential use of allo- over egocentric search strategies in the Morris water maze. TRN-dependent thalamic inhibition is thus an integral part of limbic navigational circuits wherein it coordinates external sensory and internal HD signals to regulate the choice of search strategies during spatial navigation.
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•dPreS/RS cortices send a monosynaptic glutamatergic projection to anterodorsal TRN cells•This projection leads to feedforward inhibition of anterior thalamic cells•Chemogenetic TRN silencing deteriorates thalamic head-direction cell tuning•Chemogenetic TRN silencing alters search strategies in the Morris water maze
Presubicular-retrosplenial cortices (PreS-RSC) contribute to cue-guided spatial navigation systems. Vantomme et al. show that an excitatory glutamatergic projection from PreS-RSC recruits anterodorsal thalamic reticular nucleus-mediated feedforward inhibition to sharpen mouse thalamic head direction cell tuning and to guide navigational search strategies in the Morris water maze.