Place-cell capacity and volatility with grid-like inputs.

Man Yi Yim,Lorenzo A Sadun,Thibaud Taillefumier,Ila R Fiete

doi:10.7554/elife.62702

Abstract

What factors constrain the arrangement of the multiple fields of a place cell? By modeling place cells as perceptrons that act on multiscale periodic grid-cell inputs, we analytically enumerate a place cell's repertoire - how many field arrangements it can realize without external cues while its grid inputs are unique - and derive its capacity - the spatial range over which it can achieve any field arrangement. We show that the repertoire is very large and relatively noise-robust. However, the repertoire is a vanishing fraction of all arrangements, while capacity scales only as the sum of the grid periods so field arrangements are constrained over larger distances. Thus, grid-driven place field arrangements define a large response scaffold that is strongly constrained by its structured inputs. Finally, we show that altering grid-place weights to generate an arbitrary new place field strongly affects existing arrangements, which could explain the volatility of the place code.

Highlights

As animals run around in a small familiar environment, hippocampal place cells exhibit localized firing fields at reproducible positions, with each cell typically displaying at most a single firing field (O’Keefe and Dostrovsky, 1971; Wilson and McNaughton, 1993)
We show analytically that each place cell can realize a large repertoire of arrangements across all possible space where the grid inputs are unique
We show that the capacity of a place cell or spatial range over which all field arrangements can be realized equals the sum of distinct grid periods, a small fraction of the range of positions uniquely encoded by grid-like inputs

Summary

Introduction

As animals run around in a small familiar environment, hippocampal place cells exhibit localized firing fields at reproducible positions, with each cell typically displaying at most a single firing field (O’Keefe and Dostrovsky, 1971; Wilson and McNaughton, 1993). A more detailed characterization of possible structure in these responses is both experimentally and theoretically lacking, and we hypothesize that there might be structure imposed by grid cells in place field arrangements, especially when spatial cues are sparse or unavailable Our motivation for this hypothesis arises from the following reasoning: grid cells (Hafting et al, 2005) are a critical spatially tuned population that provides inputs to place cells. Their codes are unique over very large ranges due to their modular, multi-p eriodic structure (Fiete et al, 2008; Sreenivasan and Fiete, 2011; Mathis et al, 2012). It is possible that in the absence of external cues spatially reliable place fields are strongly influenced by grid-c ell inputs

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