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Active Navigation: Transformation of Spatial Representations to Planned Motor Action in the Freely Behaving Rat

  • Author(s): Olson, Jacob Michael
  • Advisor(s): Nitz, Douglas A
  • et al.
Abstract

Episodic memories are inherently spatial experiences. This is reflected in the neural implementation of space and memory in mammals, where the hippocampus is a cortical structure necessary for successful spatial navigation and encoding of episodic memories. While the spatial encoding properties in this region are well studied in rodents, the neural pathway that allows these representations to utilize this information and shape navigation behavior is not well understood. This dissertation proposes a dorsal navigation circuit from subregion CA1 of the hippocampus through to primary motor cortex. This cortical circuit passes through subiculum (SUB) and entorhinal cortex (EC), the two main output structures of hippocampus, before proceeding through retrosplenial (RSP) and posterior parietal (PPC) cortices. Both of these regions reciprocally connect to the premotor medial precentral cortex (MPC), a premotor cortex of the rat that projects directly to primary motor cortex. Evidence of the navigational utility of these regions is substantial. Lesion studies show that RSP, SUB, and EC are all necessary for full performance of hippocampus-dependent spatial navigation. PPC shows deficits more consistent with spatially driven action planning, while MPC lesions cause laterality bias in choices. Neural representations support the proposed circuit with unique spatial representations in EC, RSP, and PPC. Spatial representations in SUB and MPC, however, are not well studied in during navigation. To address the knowledge deficiencies in the proposed circuit, this dissertation contains electrophysiology studies of SUB and MPC during a complex navigation task. In SUB, a novel form of spatial encoding encoded the axis of travel. This neural population shows temporal firing properties consistent with an integrated role with hippocampus. In MPC, action encoding dominated neural representations across spatial and choice contexts. A widespread spatial signal was also present in the region. This dissertation describes the neural correlates of two cortical regions essential to a navigational control circuit. We discovered a novel spatial representation in the hippocampal formation with important navigational implications and show its link to CA1 activity through its temporal firing dynamics. Together, these studies provide further support for the existence of a dorsal cortical circuit controlling navigation in the rat.

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