A theory of joint attractor dynamics in the hippocampus and the entorhinal cortex accounts for artificial remapping and grid cell field-to-field variability.

Haggai Agmon,Yoram Burak

doi:10.7554/elife.56894

Abstract

The representation of position in the mammalian brain is distributed across multiple neural populations. Grid cell modules in the medial entorhinal cortex (MEC) express activity patterns that span a low-dimensional manifold which remains stable across different environments. In contrast, the activity patterns of hippocampal place cells span distinct low-dimensional manifolds in different environments. It is unknown how these multiple representations of position are coordinated. Here, we develop a theory of joint attractor dynamics in the hippocampus and the MEC. We show that the system exhibits a coordinated, joint representation of position across multiple environments, consistent with global remapping in place cells and grid cells. In addition, our model accounts for recent experimental observations that lack a mechanistic explanation: variability in the firing rate of single grid cells across firing fields, and artificial remapping of place cells under depolarization, but not under hyperpolarization, of layer II stellate cells of the MEC.

Highlights

The discoveries of spatially selective cells in the hippocampus (O’Keefe and J., 1971) and the medial entorhinal cortex (MEC) (Hafting et al, 2005), have opened a window into the mechanisms underlying neural coding and processing of a high-level cognitive variable, which is separated from direct sensory inputs: the brain’s estimate of an animal’s position
Experimental evidence and theoretical reasoning have suggested that the neural representation of this variable is maintained by multiple attractor networks in the hippocampus (Battaglia and Treves, 1998; Quirk et al, 1990; Samsonovich and McNaughton, 1997; Schlesiger et al, 2018; Wills et al, 2005) and the MEC (Burak, 2014; Burak and Fiete, 2009; Fuhs and Touretzky, 2006; Guanella et al, 2007; McNaughton et al, 2006; Stensola et al, 2012), each expressing highly restricted patterns of neural activity at the population level that are preserved across multiple environments and conditions (Gardner et al, 2019; Trettel et al, 2019; Yoon et al, 2013)
Instead of assuming a feed-forward architecture of the entorhinal-hippocampal network, we explore theoretically an alternative hypothesis, that grid cells and place cells are driven by two types of synaptic inputs (Fig. 1b): inputs arising from recurrent connectivity within each brain area that restrict activity to lie within low dimensional manifolds, and inputs arising from reciprocal connections between the MEC and the hippocampus that coordinate their joint representation of position

Summary

Introduction

The discoveries of spatially selective cells in the hippocampus (O’Keefe and J., 1971) and the medial entorhinal cortex (MEC) (Hafting et al, 2005), have opened a window into the mechanisms underlying neural coding and processing of a high-level cognitive variable, which is separated from direct sensory inputs: the brain’s estimate of an animal’s position. Experimental evidence and theoretical reasoning have suggested that the neural representation of this variable is maintained by multiple attractor networks in the hippocampus (Battaglia and Treves, 1998; Quirk et al, 1990; Samsonovich and McNaughton, 1997; Schlesiger et al, 2018; Wills et al, 2005) and the MEC (Burak, 2014; Burak and Fiete, 2009; Fuhs and Touretzky, 2006; Guanella et al, 2007; McNaughton et al, 2006; Stensola et al, 2012), each expressing highly restricted patterns of neural activity at the population level that are preserved across multiple environments and conditions (Gardner et al, 2019; Trettel et al, 2019; Yoon et al, 2013) Under this interpretation of the experimental observations, patterns of population activity in the hippocampal-entorhinal system are selected from a limited repertoire, shaped by synaptic connectivity that enforces the attractor dynamics. The functional relationship between grid cells and place cells, its relationship with recurrent connectivity within each brain region, and its role in the encoding of positions across multiple environments, remain unclear

Methods

Results

Conclusion