Abstract
During exploration, animals form an internal map of an environment by combining information about specific sensory cues or landmarks with the animal’s motion through space, a process which critically depends on the mammalian hippocampus. The dentate gyrus (DG) is the first stage of the hippocampal trisynaptic circuit where self-motion and sensory cue information are integrated, yet it remains unknown how neurons within the DG encode both cue related (“what”) and spatial (“where”) information during cognitive map formation. Using two photon calcium imaging in head fixed mice running on a treadmill, along with on-line sensory cue manipulation at specific track locations, we have identified robust sensory cue responses in DG granule cells largely independent of spatial location. Granule cell cue responses are stable for long periods of time, selective for the modality of the stimulus and accompanied by strong inhibition of the firing of other active neurons. At the same time, there is a smaller fraction of neurons whose firing is spatially tuned but insensitive to the presentation of nearby cues, similar to traditional place cells. These results demonstrate the existence of “cue cells” in addition to the better characterized “place cells” in the DG, an important heterogeneity that has been previously overlooked. We hypothesize that the granule cell population may support multiple channels of spatial and non-spatial information that contribute distinctly to local and down-stream computations and impact the role of the dentate gyrus in spatial navigation and episodic memory.
Highlights
Despite high velocity dependence of dentate gyrus (DG) activity in freely running mice (Supplementary Fig. 1a), there were no significant differences in the fraction of spatially selective neurons or their mean firing rates in mice running on the motorized treadmill compared to mice advancing the treadmill belt through self-driven locomotion (Supplementary Fig. 1b, c), mean spatial tuning was higher in mice running on the motorized treadmill (Supplementary Fig. 1d). 104 Granule Cell Cue Responses 105 106 To investigate the relationship between discrete sensory cues and spatial representations within the DG, we introduced a 1s odor pulse delivered in the middle of the track on each lap as a dynamic spatial cue, in addition to a tactile cue at the lap boundary
While cue cell responses were not present initially, they emerged rapidly during the first exposures to a cue while place cell responses emerged more slowly. These findings suggest that dentate cue cells stably represent basic features of sensory cues in an environment, while place cells constitute a more dynamic population that gradually adapts to current conditions, for example, by integrating between stable cues in order to provide an accurate estimate of the animal’s location when no cues are present37. 357 Heterogeneous properties of Granule Cells 358 359 The robust and consistent nature of GC cue responses suggests that cue-selective populations may have been present in previous experiments recording DG activity in vivo, the lack of precise stimulus control made it impossible to distinguish cue-responsive versus place[362] responsive components[5,6,38]
We found that DG cue cells were largely stable when recorded over long periods of time, with different cue positions, or in different room contexts, while place cells were not. 373 Previous work has demonstrated that the two major long range inputs to the dentate gyrus, the lateral and medial entorhinal cortex (LEC and MEC), are involved with processing functionally distinct information[9,10]
Summary
14 15 During exploration, animals form an internal map of an environment by combining information about specific sensory cues or landmarks with the animal’s motion through space, a process which critically depends on the mammalian hippocampus. The dentate gyrus (DG) is the first stage of the hippocampal trisynaptic circuit where self-motion and sensory cue information are integrated, yet it remains unknown how neurons within the DG encode both cue related (“what”) and spatial (“where”) information during cognitive map formation. There is a smaller fraction of neurons whose firing is spatially tuned but insensitive to the presentation of nearby cues, similar to traditional place cells. These results demonstrate the existence of “cue cells” in addition to the better characterized “place cells” in the DG, an important heterogeneity that has been previously overlooked. We hypothesize that the observed diversity of representations within the granule cell population may support parallel processing of complementary sensory and spatial information and impact the role of the dentate gyrus in spatial navigation and episodic memory
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