Extraction and encoding of spatial relationships in the retrosplenial cortex

Complex behavior demands interactions between an animal and its immediate environment. Spatial relationships are a critical component of nearly all such interactions. Accordingly, there exist distinct neural systems that construct and store representations of space. To effectively generate and utilize these spatial mappings, coordination must occur between cortical regions important for sensory processing and sub-cortical spatial systems, such as the hippocampus (HPC). The retrosplenial cortex (RSC) is a candidate structure to facilitate this coordination process, as it is anatomically positioned between the HPC formation and neocortex. To investigate the role of RSC in spatial cognition, in vivo electrophysiological recordings were performed in rats during spatial navigation tasks. First, the spatial reference frames that influence RSC neuron firing were assessed in rats running routes placed at different environmental locations. RSC neurons encoded conjunctions between the animal’s position in the environment, position within a trajectory, and action state. Conjunctive sensitivity to multiple spatial variables suggested the region could interrelate representations encoded in distinct coordinate systems. In a second experiment, rats traversed a route with recurrent structure. Individual RSC neurons exhibited periodic activation patterns on the route that repeated across analogous route segments. Simultaneously, RSC ensembles defined a framework for the encoding of route segment positions relative to the whole. The nature of the firing activity provided a novel metric of distance from each route position to all others. Finally, neurophysiological signatures of interaction between RSC and HPC were identified. RSC neurons exhibited rhythmic spiking activity at temporal frequencies observed in HPC. These neurons, as well as those without rhythmic firing, could be temporally synchronized with synaptic inputs to the HPC. Additional interregional population interactions were observed during transient excitatory events in the HPC. This work elucidates unique functions of RSC in transforming between spatial coordinate systems and parcellating complex space into sub-components. The experiments also identify the existence of novel symmetrical spatial activation patterns that construct a distributed distance code of the animal’s position from fixed points within a linear environment. Collectively, results from these studies indicate that RSC is a powerful hippocampal-cortical conduit capable of important computations relevant to spatial cognition