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.
Highlights
The hippocampal formation is thought to maintain a metric representation of space that preserves distances between represented locations, sometimes referred to as a cognitive map (O’Keefe and Nadel, 1978; O’Keefe and Dostrovsky, 1971)
We implemented a computational model of border cell-grid cell interactions which reproduced these dynamics. These simulations further demonstrated that boundary-tethered shifts in grid phase can interact with the particular path of the navigator to give rise to grid scale-dependent rescaling and local distortions of the time-averaged grid pattern, as observed experimentally (Barry et al, 2007; Stensola et al, 2012; Krupic et al, 2018). These results demonstrate that geometric deformations of a familiar environment induce history-dependent shifts in grid phase and implicate border cell-grid cell interactions as a potential source of these dynamics
To test whether boundary-tethered shifts in grid phase are observed during environmental deformations, we reanalyzed data from two classic deformation studies ((Barry et al, 2007) and (Stensola et al, 2012))
Summary
The hippocampal formation is thought to maintain a metric representation of space that preserves distances between represented locations, sometimes referred to as a cognitive map (O’Keefe and Nadel, 1978; O’Keefe and Dostrovsky, 1971). Results of environmental deformation experiments have led to the belief that this metric is fundamentally malleable (Barry et al, 2007; Krupic et al, 2016; Stensola et al, 2012; Krupic et al, 2018) In these experiments, neural activity is recorded as a rat explores a familiar environment that has been modified by stretching, compressing, or removing/ inserting chamber walls. Often described as ‘rescaling’, these distortions have been taken to suggest that the spatial metric of the cognitive map can be reshaped by altering environmental geometry (Barry et al, 2007; Sheynikhovich et al, 2009; Raudies et al, 2016) This interpretation assumes that the distortions observed in the time-averaged rate maps of grid and place cells reflect fixed changes to the underlying spatial code that are independent of the movement history of the navigator. We present results that challenge this assumption, and indicate that the grid cell spatial metric undergoes dynamic history-dependent phase shifts during environmental deformations
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