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

Dajung Jung,Soyoun Kim,Farnaz Sharif,Daesoo Kim,Sebastien Royer,Anvar Sariev

doi:10.1038/s41598-019-45983-6

Abstract

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.

Highlights

The dentate gyrus (DG) is critical for detecting changes in environments; 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
We showed that spatial representations reconfigure differently for GCs and MCs in ways that are consistent with MCs detecting changes first, GCs operating as a competitive network, and MCs enabling the spreadout of GC remapping in locations distant from the cue
The electrode position in the DG was assessed by the profile of local field potential (LFP) type 2 dentate spikes (DS2s), whose polarity is positive in the hilus and reverses above the granule cell layer[25,40] (Fig. 1b), and confirmed by the concentration of recorded cells below the DS2 reversal point and the detection of optogenetic cell responses

Summary

Introduction

The dentate gyrus (DG) is critical for detecting changes in environments; 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. 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. Mossy cells (MCs) exhibit activity patterns sensitive to changes in local cues[25,26] and are hypothesized to convey a novelty signal, which could help transform GC representations via MC-to-GC excitation and disynaptic inhibition[27,28,29]

Methods

Results

Conclusion