Neural Mechanisms of Spatial Reorientation: How We Regain Our Bearings when Lost

Reorientation, the process of regaining one's bearings when lost, is a critical navigational process for finding food, shelter, or other resources. Yet, the cognitive architecture of this navigational process remains debated. On one hand, the shape of the surrounding environment appears to be the predominant cue during reorientation, but research has shown that under certain circumstances, other directionally informative features are used. In this dissertation, the neural substrates of this navigational task are probed to evaluate the use of environmental geometry vs features during reorientation. The first chapter of this dissertation will explore how disoriented mice reorient when they must not only recover their facing direction, but also establish the reorientation context. We demonstrate that in a two-context reorientation paradigm, disoriented mice can learn to use the directional value of featural information used for context recognition for heading retrieval. Using single-unit and calcium-imaging recordings, this chapter will probe the neuronal activity of hippocampal CA1 as mice become experienced in this task. Specifically, this chapter explores the neural representation of heading retrieval and context recognition and how these representations are modulated by experience. The second chapter of this dissertation aims to uncover the origin of the representations of environmental geometry used during reorientation (i.e., before featural information is incorporated with heading retrieval). Moreover, we show that with training, mice stop using the geometry and switch to a feature-based reorientation strategy. We use chemogenetic approaches to probe the role of the retrosplenial cortex across training on a single-context reorientation paradigm and show that the retrosplenial cortex is especially important for reorientation using geometry. We use optogenetic approaches to probe the functional role of long-range GABAergic projections from hippocampal CA1 to retrosplenial cortex in suppressing spatial representations to allow feature-guided reorientation. We use single-unit and calcium-imaging to evaluate how spatial representations in retrosplenial cortex evolve from geometry-based to feature-based reorientation.