Exploring how spatial learning can affect the firing of place cells and head direction cells: the influence of changes in landmark configuration and the development of goal-directed spatial behaviour.

Abstract

Rats learn to navigate to a specific location faster in a familiar environment (Keith and Mcvety 1988). It has been proposed that place learning does not require specific reward signals, but rather, that it occurs automatically. One of the strongest pieces of evidence for the automatic nature of place learning comes from the observation that place and head direction cells reference their receptive fields to prominent landmarks in an environment without needing a reward signal (O’Keefe and Conway 1978; Taube et al. 1990b). It has also been proposed that an allocentric representation of an environment would be bound to the landmarks with the greatest relative stability to guide its orientation (O’Keefe and Nadel 1978). The first two parts of this thesis explore whether place and head direction cells automatically use the most coherent landmarks for orientation. Head direction cells have been shown to orient their preferred firing directs coherently when being exposed to conflicting landmarks in an environment (Yoganarasimha et al. 2006). A model of head direction cells was thus used to explore the necessary mechanisms required to implement an allocentric system that selects landmarks based on their relative stability. We found that the simple addition of Hebbian projections combined with units representing the orientation of landmarks to the head direction cell system is sufficient for the system to exhibit such a capacity. We then recorded both entorhinal head direction cells and CA1 place cells and at the same time subjected the rats to repeated experiences of landmark conflicts. During the conflicts a subset of landmarks always maintained a fixed relative relationship with each other. We found that the visual landmarks retained their ability to control the place and head direction cells even after repeated experience of conflict and that the simultaneously recorded place cells exhibited coherent representations between conflicts. However, the ’stable landmarks’ did not show significantly greater control over the place and head direction cells when comparing to the unstable landmarks. This argues against the hypothesis that the relative stability between landmarks is encoded automatically. We did observe a trend that, with more conflict experience, the ’stable landmarks’ appeared to exert greater control over the cells. The last part of the thesis explores whether goal sensitive cells (Ainge et al. 2007a) discovered from CA1 of hippocampus are developed due to familiarity with the environment or from the demands for rats to perform a win-stay behaviour. We used the same win-stay task as in Ainge et al. and found that there were few or no goal sensitive cells on the first day of training. Subsequent development of goal sensitive activity correlated significantly with the rat’s performance during the learning phase of the task. The correlation provides support to the hypothesis that the development of goal sensitive cells is associated to the learning of the win-stay task though it does not rule out the possibility that these goal sensitive cells are developed due to the accumulated experience on the maze. In summary, this thesis explores what kind of spatial information is encoded by place and head direction cells and finds that relative stability between landmarks without a reward signal is not automatically encoded. On the other hand, when additional information is required to solve a task, CA1 place cells adapt their spatial code to provide the necessary information to guide successful navigation.