A. David Redish

Beyond the Cognitive Map: Contributions to a Computational Neuroscience Theory of Rodent Navigation Degree Type: Ph.D. in Computer Science
Advisor(s): David Touretzky
Graduated: August 1997

Abstract:

Rodent navigation is a unique domain for studying information processing in the brain because there is a vast literature of experimental results at many levels of description, including anatomical, behavioral, neurophysiological, and neuropharmacological. This literature provides many constraints on candidate theories. This thesis presents contributions to a theory of how rodents navigate as well as an overview of that theory and how it relates to the experimental literature.

In the first half of the thesis, I present a review and overview of the rodent navigation literature, both experimental and theoretical. The key claim of the theory is that navigation can be divided into two categories: taxon/praxic navigation and locale navigation (O'Keefe and Nadel, 1978), and that locale navigation can be understood as an interaction between five subsystems: local view, head direction, path integration, place code, and goal memory (Redish and Touretzky, 1997). I bring ideas together from the extensive work done on rodent navigation over the last century to show how the interaction of these systems forms a comprehensive, computational theory of navigation. This comprehensive theory has implications for an understanding of the role of the hippocampus, suggesting that it shows three different modes: storage, recall, and replay.

In the second half of the thesis, I show specific contributions to this overall theory.

• I report the first simulation of the head direction system that can track multiple head direction speeds accurately. The simulations show that the theory implies that head direction tuning curves in the anterior thalamic nuclei should deform during rotations. This observation has been confirmed experimentally by Blair et al. (1997)
• By examining the computational requirements and the anatomical data, I suggest that the anatomical locus of the path integrator is in a loop comprised of the subiculum, the parasubiculum, and the superficial entorhinal cortex. This contrasts with other hypotheses of the anatomical locus of path integration (e.g. hippocampus, McNaughton et al. 1996) and predicts that the hippocampus should not be involved in path integration. This prediction has been recently tested and confirmed by Alyan et al. (1997).
• I present simulations demonstrating the viability of the three-mode hippocampal proposal, including storage and recall of locations within single environments, with ambiguous inputs, and in multiple environments.
• I present simulations demonstrating the viability of the dual-role hippocampus (recall and replay), showing that the two modes can coexist within the hippocampus even though the two roles seem to require incompatible connection matrices.

In addition, I present simulations of specific experiments, including

• a simulation of the recent result from Barnes et al. (1997), showing that the model produces a bimodality in the correlations of representations of an environment in animals with deficient LTP. These simulations show that the Barnes et al. (1997) result does not necessarily imply that the intra-hippocampal connections are pre-wired to form separate charts as suggested by Samsonovich (1997).
• a simulation of Sharp et al.\s (1990) data on the interaction between entry point and external cues, showing the first simulations capable of replicating all the single place field conditions reported by Sharp et al.
• simulations of Cheng (1986) and Margules and Gallistel (1988) showing the importance of disorientation in self-localization.
• simulations of Morris et al. (1981), showing that the model can replicate navigation in the water maze.
• simulations of Collett et al. (1986) and our own gerbil navigation results, showing that the model can replicate a number of reactions to different manipulations of landmark arrays.

Thesis Committee:
David S. Touretzky (Chair)
James L. McClelland
David C. Plaut
Bruce L. McNaughton (University of Arizona)

James Morris, Head, Computer Science Department
Raj Reddy Dean, School of Computer Science

Keywords:
Theoretical neuroscience, computational neuroscience, spatial cognition, place cell, head direction cell, path integration