The statistical structure of the hippocampal code for space as a function of time, context, and value

Abstract

Hippocampal activity represents many behaviorally important variables, including context, an animal's location within a given environmental context, time, and reward. Here we used longitudinal calcium imaging in mice, multiple large virtual environments, and differing reward contingencies to derive a unified probabilistic model of hippocampal CA1 representations centered on a single feature -the field propensity. Each cell's propensity governs how many place fields it has per unit space, predicts its reward-related activity, and is preserved across distinct environments and over months. The propensity is broadly distributed-with many low, and some very high, propensity cells -and thus strongly shapes hippocampal representations. The result is a range of spatial codes, from sparse to dense. Propensity varied ~10-fold between adjacent cells in a salt-and-pepper fashion, indicating substantial functional differences within a presumed cell type. The stability of each cell's propensity across conditions suggests this fundamental property has anatomical, transcriptional, and/or developmental origins.

Changing reward expectation transforms spatial encoding and retrieval in the hippocampus

“…These results provide strong evidence that spatial representations of environments are not value-free as has been suggested (Duvelle et al, 2019;Tabuchi et al, 2003), but instead value determines the structure and dynamics of spatial representations in CA1. Reward contingencies in navigation tasks have been shown to modulate place cells (Danielson et al, 2016;Gauthier and Tank, 2018;Lee et al, 2012;Lee et al, 2006;Lee et al, 2019;Martig and Mizumori, 2011;Tryon et al, 2017;Wikenheiser and Redish, 2011). Most studies in this area either alter reward magnitudes or move reward locations, and many times include a decision-making component in their behavioral task.…”

Reversible Loss of Hippocampal Function in a Mouse Model of Demyelination/Remyelination

“…For hippocampal window implantation, we slightly modified a previously described procedure (Dombeck et al, 2010;Lee et al, 2019). Thy1-jRGECO1a line 8.31 mice were anesthetized using isoflurane (2.5-3% for induction, 1.5% during surgery) on a 37 • C heating pad.…”

“…In order to further investigate the prevalence and time course of CA1 neuronal activity modulations, we conducted additional experiments for longitudinal optical recording of GECI signal from the hippocampus of lightly anesthetized mice (n = 7 mice, 10-17 weeks old when implanted with an optical window; mice 1, 4, and 7 were males; mice 2, 3, 5, and 6 were females). Optical recording from CA1 cells usually requires removal of the cortical tissue on top of the recorded area (Dombeck et al, 2010;Ziv et al, 2013;Lee et al, 2019). Recordings from the DG area have also required removal of the CA1 region, causing severe damage to the hippocampal circuit (Danielson et al, 2016(Danielson et al, , 2017.…”

Mechanisms of neural organization and rhythmogenesis during hippocampal and cortical ripples

“…Statistical models of place field allotment in large, featureless linear tracks show that field distribution can be well explained by a model in which any given cell lays down a place field in a random location at a fixed probability, which varies across neurons [63]. More recent studies show that this probability is fixed across environments and over weeks of recordings, suggesting that this heterogeneity is driven by differences in intrinsic neural excitability (potentially including number/strength of synaptic inputs) [64]. In support of this hypothesis, neurons that had a place field in a novel environment showed a lower threshold to spiking with intracellular current injection prior to that first-time exposure [65].…”