Time Makes Space: Emergence of Place Fields in Networks Encoding Temporally Continuous Sensory Experiences

TL;DR

This paper demonstrates that place cells can emerge in neural networks trained on temporally continuous sensory experiences, reproducing key hippocampal phenomena and suggesting a link between temporal continuity and spatial mapping.

Contribution

It introduces a recurrent autoencoder model that develops place fields from continuous sensory episodes, highlighting the role of temporal continuity in spatial representation emergence.

Findings

Place fields emerge in the model with activity constraints.

Model reproduces remapping and orthogonality of spatial maps.

Place fields are robust across different room shapes and exhibit drift.

Abstract

The vertebrate hippocampus is believed to use recurrent connectivity in area CA3 to support episodic memory recall from partial cues. This brain area also contains place cells, whose location-selective firing fields implement maps supporting spatial memory. Here we show that place cells emerge in networks trained to remember temporally continuous sensory episodes. We model CA3 as a recurrent autoencoder that recalls and reconstructs sensory experiences from noisy and partially occluded observations by agents traversing simulated rooms. The agents move in realistic trajectories modeled from rodents and environments are modeled as high-dimensional sensory experience maps. Training our autoencoder to pattern-complete and reconstruct experiences with a constraint on total activity causes spatially localized firing fields, i.e., place cells, to emerge in the encoding layer. The emergent place fields reproduce key aspects of hippocampal phenomenology: a) remapping (maintenance of and reversion to distinct learned maps in different environments), implemented via repositioning of experience manifolds in the network's hidden layer, b) orthogonality of spatial representations in different arenas, c) robust place field emergence in differently shaped rooms, with single units showing multiple place fields in large or complex spaces, and d) slow representational drift of place fields. We argue that these results arise because continuous traversal of space makes sensory experience temporally continuous. We make testable predictions: a) rapidly changing sensory context will disrupt place fields, b) place fields will form even if recurrent connections are blocked, but reversion to previously learned representations upon remapping will be abolished, c) the dimension of temporally smooth experience sets the dimensionality of place fields, including during virtual navigation of abstract spaces.