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

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 multisensor...

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Bibliographic Details
Published in:Cell reports (Cambridge) 2020-06, Vol.31 (10), p.107747-107747, Article 107747
Main Authors: Vantomme, Gil, Rovó, Zita, Cardis, Romain, Béard, Elidie, Katsioudi, Georgia, Guadagno, Angelo, Perrenoud, Virginie, Fernandez, Laura M.J., Lüthi, Anita
Format: Article
Language:English
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
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Summary: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. [Display omitted] •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.
ISSN:2211-1247
2211-1247
DOI:10.1016/j.celrep.2020.107747