Dentate granule and mossy cells exhibit distinct spatiotemporal responses to local change in a one-dimensional landscape of visual-tactile cues

The dentate gyrus (DG) is critical for detecting changes in environments; however, how granule cells (GCs) and mossy cells (MCs), the two excitatory cell types of the DG, respond to small changes in the object layout is unclear. Here, we recorded GCs and MCs, identified by spike feature and optogenetic tagging, as mice ran on a treadmill belt enriched with visual-tactile cues. We observed that fixing a new cue on the belt induced a reconfiguration of GC and MC spatial representations via the emergence, extinction and rate alteration of firing fields. For both GCs and MCs, the response was maximal near the cue and spread over the entire belt. However, compared to the GC response, the MC response was stronger and more immediate, peaked at a slightly earlier belt position, and exhibited a transient component reminiscent of neuromodulatory activity. A competitive neural network model reproduced the GC response contingent on both the introduction of new object-vector inputs and the reconfiguration of MC activity, the former being critical for spreading the GC response in locations distant from the cue. These findings suggest that GCs operate as a competitive network and that MCs precede GCs in detecting changes and help expand the range of GC pattern separation.