Since their discovery in the early ‘70s1, hippocampal place cells have been studied in numerous animal and human spatial memory paradigms2–4. These pyramidal cells, along with other spatially tuned types of neurons (e.g. grid cells, head direction cells), are thought to provide the mammalian brain a unique spatial signature characterizing a specific environment, and thereby a memory trace of the subject’s place5. While grid and head direction cells are found in various brain regions, only few hippocampal-related structures showing ‘place cell’-like neurons have been identified6,7, thus reinforcing the central role of the hippocampus in spatial memory. Concurrently, it is increasingly suggested that visual areas play an important role in spatial cognition as recent studies showed a clear spatial selectivity of visual cortical (V1) neurons in freely moving rodents8–10. We therefore thought to investigate, in the rat, such spatial correlates in a thalamic structure located one synapse upstream of V1, the dorsal Lateral Geniculate Nucleus (dLGN), and discovered that a substantial proportion (ca. 30%) of neurons exhibits spatio-selective activity. We found that dLGN place cells maintain their spatial selectivity in the absence of visual inputs, presumably relying on odor and locomotor inputs. We also found that dLGN place cells maintain their place selectivity across sessions in a familiar environment and that contextual modifications yield separated representations. Our results show that dLGN place cells are likely to participate in spatial cognition processes, creating as early as the thalamic stage a comprehensive representation of one given environment.

Spatial cognition is an important model system with which to investigate how sensory signals are transformed into cognitive representations. Head direction cells, found in several cortical and subcortical regions, fire when an animal faces a given direction and express a global directional signal which is anchored by visual landmarks and underlies the "sense of direction". We investigated the interface between visual and spatial cortical brain regions and report the discovery that a population of neurons in the dysgranular retrosplenial cortex, which we co-recorded with classic head direction cells in a rotationally symmetrical twocompartment environment, were dominated by a local visually defined reference frame and could be decoupled from the main head direction signal. A second population showed rotationally symmetric activity within a single sub-compartment suggestive of an acquired interaction with the head direction cells. These observations reveal an unexpected incoherence within the head direction system, and suggest that dysgranular retrosplenial

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