Entorhinal-retrosplenial circuits for allocentric-egocentric transformation of boundary coding.

Joeri Bg Van Wijngaarden,Susanne S Babl,Hiroshi T Ito

doi:10.7554/elife.59816

Joeri Bg Van Wijngaarden, Susanne S Babl + Show 1 more

Open Access

https://doi.org/10.7554/elife.59816

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Abstract

Spatial navigation requires landmark coding from two perspectives, relying on viewpoint-invariant and self-referenced representations. The brain encodes information within each reference frame but their interactions and functional dependency remains unclear. Here we investigate the relationship between neurons in the rat's retrosplenial cortex (RSC) and entorhinal cortex (MEC) that increase firing near boundaries of space. Border cells in RSC specifically encode walls, but not objects, and are sensitive to the animal's direction to nearby borders. These egocentric representations are generated independent of visual or whisker sensation but are affected by inputs from MEC that contains allocentric spatial cells. Pharmaco- and optogenetic inhibition of MEC led to a disruption of border coding in RSC, but not vice versa, indicating allocentric-to-egocentric transformation. Finally, RSC border cells fire prospective to the animal's next motion, unlike those in MEC, revealing the MEC-RSC pathway as an extended border coding circuit that implements coordinate transformation to guide navigation behavior.

Highlights

Animals use landmarks in the environment as references to identify the self’s position and a destination in space
By applying a metric of the earth mover’s distance (EMD), we identified a subpopulation of neurons in retrosplenial cortex (RSC) that increase their firing rates depending on the distance of nearby walls, supporting boundary representations in RSC
We found that firing of RSC border cells is specific to boundaries that impede the movement of animals, while an object introduced into the maze does not elicit a corresponding change of activity nearby

Summary

Introduction

Animals use landmarks in the environment as references to identify the self’s position and a destination in space. For example, are able to discriminate positions within an open field arena by relying on distal cues in the room, allowing them to navigate to a desired location (Morris, 1981) This ability is manifested in the activity of neurons that fire at particular locations in space, such as place cells or grid cells (Hafting et al, 2005; O’Keefe and Dostrovsky, 1971), and population activity of place cells can distinguish nearby positions at several centimeter resolution in an open field arena (Brown et al, 1998). The presence of dedicated representations of environmental borders in the hippocampus and parahippocampal regions implies a pivotal role of boundary information in generating accurate spatial representations in the brain In accordance with this idea, border cells in MEC develop earlier than grid cells after birth, exhibiting adult-like firing fields at postnatal days 16– 18 when grid cells still exhibit immature irregular firing fields (Bjerknes et al, 2014). It has further been shown that position errors of firing fields of grid cells accumulate after the animal leaves a wall of an open field arena, suggesting an error-correcting role of environmental boundaries for internal spatial representations (Hardcastle et al, 2015)

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