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During exploration, animals form an internal map of an environment by combining information about landmarks and the animal’s movement, a process that depends on the hippocampus. The dentate gyrus (DG) is the first stage of the hippocampal circuit where self-motion (“where”) and sensory cue information (“what”) are integrated, but it remains unknown how DG neurons encode this information during cognitive map formation. Using two-photon calcium imaging in mice running on a treadmill along with online cue manipulation, we identify robust sensory cue responses in DG granule cells. Cue cell responses are stable, stimulus-specific, and accompanied by inhibition of nearby neurons. This demonstrates the existence of “cue cells” in addition to better characterized “place cells” in the DG. We hypothesize that the DG supports parallel channels of spatial and non-spatial information that contribute distinctly to downstream computations and affect roles of the DG in spatial navigation and episodic memory.
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•Mouse dentate granule cells respond strongly to spatial sensory cues on a treadmill•Cue cells emerge faster and are more stable than place cells•Cue cells are weakly modulated by location and place cells by spatially invariant cues•Cue responses lead to inhibition of other granule cells in the local population
Tuncdemir et al. describe how information about spatial landmarks and movement is encoded in the first stage of the hippocampus, the dentate gyrus. The authors show that, rather than being a simple population of “place cells,” the dentate gyrus is also prominently characterized by “cue cells” independent of location.