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

Gil Vantomme,Anita Luthi,Laura Marie Justine Fernandez,Elidie Béard,Angelo Guadagno,Virginie Perrenoud,Romain Cardis,Zita Rovó,Georgia Katsioudi

doi:10.2139/ssrn.3469826

Abstract

To navigate in space, an animal must reference external sensory landmarks to the spatial orientation of its body and head. Circuit and synaptic mechanisms that integrate external cues with internal head-direction (HD) signals to drive navigational behavior remain, however, poorly described. We identify an excitatory synaptic projection from the presubiculum and retrosplenial cortex to the anterodorsalmost sector of the thalamic reticular nucleus (TRN), so far classically implied in gating sensory information flow. Projections to TRN showed driver characteristics and involved AMPA/NMDA-type glutamate receptors that initiated TRN cell burst discharge and feedforward inhibition of anterior thalamic nuclei, where HD-tuned cells relevant for egocentric navigation reside. Chemogenetic anterodorsal TRN inhibition broadened the tuning of thalamic HD cells and compromised egocentric search strategies in the Morris water maze. Besides sensory gating, TRN-dependent thalamic inhibition is an integral part of limbic navigational circuits to recruit HD-cell-dependent search strategies during spatial navigation.

Highlights

To reach a goal, search for food, or avoid a predator, navigation in space is essential
Sensory cortices elaborate information they receive from the sensory organs, and they interact with widespread thalamo-cortico-hippocampal networks that contain internal representations of space and body orientation to guide navigation (Hinman et al, 2018; Velez-Fort et al, 2018)
We found punctate staining in the adjacent anterodorsal thalamic nucleus (AD), laterodorsal (LD), and in the centrolateral (CL) nuclei of the thalamus (Figure 1A2, identified in 3 out of 4 injections), consistent with prior tracing studies (Gonzalo-Ruiz and Lieberman, 1995a, 1995b; Lozsadi, 1995; Pinault and Desche^nes, 1998)

Summary

Introduction

Search for food, or avoid a predator, navigation in space is essential. Animals rely on sensory landmarks in the environment to monitor and adapt their path and body orientation in space. Sensory cortices elaborate information they receive from the sensory organs, and they interact with widespread thalamo-cortico-hippocampal networks that contain internal representations of space and body orientation to guide navigation (Hinman et al, 2018; Velez-Fort et al, 2018). Sensory guided spatial navigation may be engaged at subcortical levels (Hinman et al, 2018; Knudsen, 2018), which could be critical to adapt navigational strategies in a rapidly changing environment. A major site for subcortical gating of external sensory stimuli is the inhibitory thalamic reticular nucleus (TRN) that shows a unique anatomical positioning at the interface between sensory thalamic nuclei and cortex (Crabtree, 2018; Pinault, 2004; Scheibel and Scheibel, 1966). Activity in TRN controls the gain of sensory inputs (Le Masson et al, 2002), sharpens receptive fields in thalamic sensory nuclei (Lee et al, 1994; Soto-Sanchez et al, 2017), underlies sensory selection in divided attentional tasks (Ahrens et al, 2015; Wimmer et al, 2015), and is involved in sensory induced flight responses (Dong et al, 2019) and in extinction of cued fear conditioning (Lee et al, 2019)

Methods

Findings

Discussion

Conclusion