A Tale of Two Direction Codes in Rat Retrosplenial Cortex: Uncovering the Neural Basis of Spatial Orientation in Complex Space

Abstract

Head direction (HD) cells only become active whenever a rat faces one direction and stay inactive when it faces others, producing a unimodal activity distribution. Working together in a network, HD cells are considered the neural basis supporting a sense of direction. The retrosplenial cortex (RSC) is part of the HD circuit and contains neurons that express multiple spatial signals, including a pattern of bipolar directional tuning – as recently reported in rats exploring a rotationally symmetric two-compartment space. This suggests an unexplored mechanism of the neural compass. In this thesis, I investigated whether the association between the two-way firing symmetry and twofold environment symmetry reveals a general environment symmetry-encoding property of these RSC neurons. I recorded RSC neurons in environments having onefold, twofold and fourfold symmetry. The current study showed that RSC HD cells maintained a consistent global signal, whereas other RSC directional cells showed multi-fold symmetric firing patterns that reflected environment symmetry, not just globally (across all sub-compartments) but also locally (within each sub-compartment). The analyses also showed that the pattern was independent of egocentric boundary vector coding but represented an allocentric spatial code. It means that these RSC cells use environmental cues to organise multiple singular tuning curves which sometimes are combined to form a multidirectional pattern, likely via an interaction with the global HD signal. Thus, both local and global environment symmetry are encoded by local firing patterns in subspaces. This interestingly suggests cognitive mapping and abstraction of space beyond immediate perceptual bounds in RSC. The data generated from this study provides important insights for modelling of direction computation. Taken together, I discuss how having two types of direction codes in RSC may help us to orient more accurately and flexibly in complex and ambiguous space

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