Thalamic head-direction cells are organized irrespective of their inputs

Continuous attractor networks support various cognitive functions yet the neuronal dynamics and circuits supporting these dynamics in vivo remain unclear. The HD circuit is a canonical example of such network and HD cells each fire for a specific direction of the animal’s head. In the anterodorsal nucleus of the thalamus (ADn), HD cells maintain their mutual coordination during sleep, when sensory inputs are virtually absent, supporting the view of an attractor-driven system. The rigid organization of HD cell activity in the ADN begs the question of the origin of these structured patterns. The upstream structure, the lateral mammillary nucleus (LMN), is a central component of the HD signal generator circuit, though of supporting the attractor properties of the network. We thus investigated the organization of LMN activity across brain states, and its relationship to ADn. To this end, we recorded ADN-LMN neuronal ensembles during exploration and sleep. Here we show that during non Rapid-Eye-Movement sleep (nREM), LMN-HD cells coordination was reduced while simultaneously recorded ADN neurons maintained the same level of mutual coherence. The decreased level of correlation in LMN resulted, at least in part, by a switch to hypersynchronous spiking activity in which neurons co-fired irrespective of their mutual preferred direction. Inter-spikes intervals (ISIs) during the transition to a preferred direction revealed a discrete activation of ADN neurons as opposed to a continuous activation of LMN neurons. Simulating a population of ADN neurons with a non-linear integration of LMN inputs was enough to replicate the enhanced coordinated activity in the ADN during nREM sleep. Our results suggest that the response property of ADN neurons is sufficient to generate attractor dynamics.