Hippocampal spike‐time correlations and place field overlaps during open field foraging

Abstract

Phase precessing place cells encode spatial information on fine timescales via the timing of their spikes. This phase code has been extensively studied on linear tracks and for short runs in the open field. However, less is known about the phase code on unconstrained trajectories lasting tens of minutes, typical of open field foraging. In previous work (Monsalve‐Mercado and Leibold, Physical Review Letters, 119, 38101 (2017)), an analytic expression was derived for the spike‐time cross‐correlation between phase precessing place cells during natural foraging in the open field. This expression makes two predictions on how this phase code differs from the linear track case: cross‐correlations are symmetric with respect to time, and they represent the distance between pairs of place fields in that the theta‐filtered cross‐correlations around zero time lag are positive for cells with nearby fields while they are negative for those with fields further apart. Here we analyze several available open field recordings and show that these predictions hold for pairs of CA1 place cells. We also show that the relationship remains during remapping in CA1, and it is also present in place cells in area CA3. For CA1 place cells of Fmr1‐null mice, which exhibit normal place fields but somewhat weaker temporal coordination with respect to theta compared to wild type, the cross‐correlations still remain symmetric but the relationship to place field overlap is largely lost. The relationship discussed here describes how spatial information is communicated by place cells to downstream areas in a finer theta‐timescale, relevant for learning and memory formation in behavioral tasks lasting tens of minutes in the open field.

Multiscale and Extended Retrieval of Associative Memory Structures in a Cortical Model of Local-Global Inhibition Balance

“…However, this kind of correlated, associative memory structure is not only found in the visual system, it is also noticeable and widely studied in hippocampus. Within a spatial environment, place cells representing nearby place fields show correlated activity ( Monsalve-Mercado and Roudi, 2020 ) and can maintain correlations in the same environment over different tasks ( Hampson et al, 1996 ), mostly because of overlapping place fields. When the environment changes, however, these correlations are typically inconsistent with one another ( Alme, et al, 2014 ), suggesting contextual cues alter or switch between different memory structures.…”

Introduction to part two of the special issue on computational models of hippocampus and related structures

“…This phenomenon of theta phase precession has been modeled by the interaction of oscillations at different frequencies for place cells (O'Keefe & Recce, 1993) and for grid cells (Burgess, 2008; Burgess, Barry, & O'Keefe, 2007). Phase coding has been used in other models of grid cells in part of this special issue (Grgurich & Blair, 2020; Monsalve‐Mercado & Roudi, 2020). There has been an ongoing comparison of the relative effectiveness of different models of grid cells (Bush & Burgess, 2020; Stella, Urdapilleta, Luo, & Treves, 2020).…”

Overview of computational models of hippocampus and related structures: Introduction to the special issue

“…These data on spike‐timing dependent plasticity (STDP) are consistent with the detailed kinetics of the NMDA receptor and associated calcium levels (Holmes & Levy, ). The important functional role of spike timing and spike‐timing dependent plasticity is addressed in the special issue paper by Monsalve‐Mercado and Roudi (). This paper presents a detailed analysis of the timing of spikes in hippocampal neurons and discusses the potential role in coding of spatial location and consolidation.…”

“…The phase of spikes can be coded in relation to the phase of field potential data without stable oscillations, as supported by recent data from bats showing phase coding without oscillations (Eliav et al, ). As noted above, the phase coding of neurons in hippocampus has also been proposed as a mechanism for generating grid cell firing (Monsalve‐Mercado & Leibold, ), as discussed in the special issue paper by Monsalve‐Mercado and Roudi ().…”