Environmental deformations dynamically shift the grid cell spatial metric

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Abstract

In familiar environments, the firing fields of entorhinal grid cells form regular triangular lattices. However, when the geometric shape of the environment is deformed, these time-averaged grid patterns are distorted in a grid scale-dependent and local manner. We hypothesized that this distortion in part reflects dynamic anchoring of the grid code to displaced boundaries, possibly through border cell-grid cell interactions. To test this hypothesis, we first reanalyzed two existing rodent grid rescaling datasets to identify previously unrecognized boundary-tethered shifts in grid phase that contribute to the appearance of rescaling. We then demonstrated in a computational model that boundary-tethered phase shifts, as well as scale-dependent and local distortions of the time-averaged grid pattern, could emerge from border-grid interactions without altering inherent grid scale. Together, these results demonstrate that environmental deformations induce history-dependent shifts in grid phase, and implicate border-grid interactions as a potential mechanism underlying these dynamics.

Data availability

All simulations were conducted with custom-written MATLAB scripts. These scripts and the simulation results presented here are available on Github at: https://github.com/akeinath/Keinath_BoundaryTetheredModel. All values generated during our reanalysis are included as source data files. All original reanalyzed data were originally reported in the following papers:1)Barry et al., 2007. Experience-dependent rescaling of entorhinal grids. https://doi.org/10.1038/nn1905;2)Stensola et al., 2012. The entorhinal map is descritized. https://doi.org/10.1038/nature11649.These data are available upon request from the corresponding authors of these papers.

Article and author information

Author details

Alexandra T Keinath

Department of Psychology, University of Pennsylvania, Philadelphia, United States

For correspondence
atkeinath@gmail.com

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-1622-7835
Russell A Epstein

Department of Psychology, University of Pennsylvania, Philadelphia, United States

Competing interests
The authors declare that no competing interests exist.
Vijay Balasubramanian

Department of Physics, University of Pennsylvania, Philadelphia, United States

For correspondence
vijay@physics.upenn.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6497-3819

Funding

National Science Foundation (PHY-1734030)

Vijay Balasubramanian

National Institutes of Health (EY022350)

Russell A Epstein

National Institutes of Health (EY022350)

Russell A Epstein

National Science Foundation (966142)

Alexandra T Keinath

National Science Foundation (PHY-584 1607611))

Vijay Balasubramanian

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.