Landmark-Based Updating of the Head Direction System by Retrosplenial Cortex: A Computational Model.

Hector J I Page,Kate J Jeffery

doi:10.3389/fncel.2018.00191

Abstract

Maintaining a sense of direction is fundamental to navigation, and is achieved in the brain by a network of head direction (HD) cells, which update their signal using stable environmental landmarks. How landmarks are detected and their stability determined is still unknown. Recently we reported a new class of cells (Jacob et al., 2017), the bidirectional cells, in a brain region called retrosplenial cortex (RSC) which relays environmental sensory information to the HD system. A subset of these cells, between-compartment (BC) cells, are directionally tuned (like ordinary HD cells) but follow environmental cues in preference to the global HD signal, resulting in opposing (i.e., bidirectional) tuning curves in opposed environments. Another subset, within-compartment (WC) cells, unexpectedly expressed bidirectional tuning curves in each one of the opposed compartments. Both BC and WC cells lost directional tuning in an open field, unlike HD cells. Two questions arise from this discovery: (i) how do these cells acquire their unusual response properties, and (ii) what are they for? We propose that bidirectional cells reflect a two-way interaction between local direction, as indicated by the visual environment, and global direction as signaled by the HD system. We suggest that BC cells receive strong inputs from visual cues, while WC cells additionally receive modifiable inputs from HD cells which, due to Hebbian coactivation of visual inputs plus two opposing sets of HD inputs, acquire the ability to fire in both directions. A neural network model instantiating this hypothesis is presented, which indeed forms both BC and WC bidirectional cells with properties similar to those seen experimentally. We then demonstrate how tuning specificity degrades when WC/BC cells are exposed to multiple directionalities, replicating the observed loss of WC and BC directional tuning in the open field. We suggest that the function of these neurons is to assess the stability of environmental landmarks, thereby determining their utility as reference points by which to set the HD sense of direction. This role could extend to the ability of the HD system to prefer distal over proximal landmarks, and to correct for parallax errors.

Highlights

The brain’s construction of an internal ‘‘map’’ of external space involves transformation from basic sensory inputs to higher-order representations, resulting in abstract concepts such as ‘‘place,’’ or ‘‘heading.’’ The study of spatial cognition can help us to understand how the brain forms such concepts, which is broadly relevant to cognition more generally
We propose a function for this network that explains the function of these three cell classes: namely, that bidirectional cells reflect a retrosplenial cortex (RSC) role in both evaluating the usefulness of environmental sensory inputs for indicating current direction, and for incorporating direction as indicated by these inputs with a sense of direction maintained by the head direction (HD) system
The present study investigated at a theoretical level how the brain uses the visual environment to establish and update the sense of direction, as reflected in the activity of HD cells

Summary

Introduction

The brain’s construction of an internal ‘‘map’’ of external space involves transformation from basic sensory inputs to higher-order representations, resulting in abstract concepts such as ‘‘place,’’ or ‘‘heading.’’ The study of spatial cognition can help us to understand how the brain forms such concepts, which is broadly relevant to cognition more generally. Environmental landmarks must be assessed for stability This necessitates an evaluation of newlyencountered landmarks relative to an internal sense of direction, so that only landmarks that have been learned as a stable source of directional information will update HD cell firing (Knierim et al, 1995; Knight et al, 2013). There is a chicken-and-egg problem—stable landmarks are used to orient the sense of direction, but the sense of direction is needed to determine whether landmarks are stable Another issue is that sensory input is initially represented relative to the body (egocentric), while an internal sense of direction is relative to the external world (allocentric; Bicanski and Burgess, 2016). Use of environmental information to set the sense of direction equates to a transformation between egocentric and allocentric spatial reference frames (Vann et al, 2009; Knight and Hayman, 2014)

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Conclusion