A Hippocampal Model for Learning and Recalling Paths: From Place Cells to Path Cells

Navigation is a foundational skill for animals. From insects to birds to mammals, many animals have developed various strategies to search for that which they require, remember its location, then safely return home. Discovering some of the techniques these animals use has yielded unique solutions for the navigational problems of artificial autonomous systems. Yet many questions remain unanswered regarding the navigational abilities that so many animals appear to possess. One such ability is path encoding and recall - learning a set of places in an environment and the connectivity between those places, then using the resulting graph or map for myriad goals. Empirical data collected over the past century indicates that some animals, and specifically rodents, are capable of behaviours difficult to reconcile with non-path-based explanations. In more recent decades, since the discovery of spatially sensitive 'place cells' in the rat brain, it has become clear that the hippocampus plays a significant role in map-based navigation. Simultaneously developing in the field of mobile autonomous systems have been algorithmic techniques to solve a similar map-based navigation problem, termed Simultaneous Localisation and Mapping (SLAM), which highlight the information-theoretical principles involved. The goal of this thesis has been to explore, using spiking neural modelling techniques, how the electrophysiological and anatomical properties of the rodent hippocampus can satisfy the theoretical requirements of an online path learning and recall system. Recognition of novelty is a key element of any memory system. In particular, it is a core component both in learning and recognising locations and in linking locations into paths. Existing studies have demonstrated learning mechanisms capable of developing appropriate unique memories, and corresponding recall mechanisms capable of ignoring random variance in the input. These features are necessary for navigational memory from a theoretical perspective, and also provide a good fit for some electrophysiological data. However these studies have not addressed the issue of when each process, learning and recall, should occur. The first part of this thesis extends existing models of the hippocampal network, incorporating the timing of individual spikes, and using this extra dimension to provide an internal novelty signal. It demonstrates how a network that matches known hippocampal anatomy can instigate a race between a teaching signal and recall signal, with the teaching signal winning the race only in the case of a novel input. Using this novelty signal, what constitutes a novel input can itself be modified dynamically, without destabilising the system. In a navigational context, individual memories can be likened to place, and sequences of such memories to paths. The predominant interpretation of the spatial selectivity of place cells is that these cells are 'coding for' the location of the animal at the time of their firing. Beyond this pure spatial selectivity, evidence demonstrates that during traversal of a cell's place field, its firing precesses with respect to the local theta oscillation - an effect termed 'theta phase precession' - and this precession is correlated with relative progression through the place field. One common interpretation of this precession effect is that it provides a greater degree of locational specificity. The remainder of this thesis explores an alternative hypothesis that place fields and theta phase precession are evidence of a path encoding and recall mechanism. A mechanism based on the known anatomy of CA3 is proposed that is consistent with many dynamical properties of the region and can explain known variations in spatial selectivity across the CA3 network. The proposed mechanism suggests that CA3 performing path encoding and recall over complete foraging ranges could be the functional justification for anatomical and dynamical variation across the region. The thesis concludes with a discussion of the implications of this theory on the interpretation of place cell data, and an outline of experimental designs for its validation.