Neural compass or epiphenomenon? Experimental and theoretical investigations into the rodent head direction system

How does the brain convert sensory information into abstract representations that can support complex behaviours? The rodent head-direction (HD) system, whose cell ensembles represent head direction in the horizontal plane, is a striking example of a “cognitive” representation without a direct sensory correlate. It can be updated by sensory inputs from different modalities, yet persists in the absence of external input. Together with cells tuned for place, the HD system is thought to be fundamental for navigation and spatial information processing. However, relatively few studies have sought to characterise the connection between the HD system and spatial behaviour directly, and their overall outcome has been inconclusive. In the experiments that make up the first part of this thesis, we approach this issue by isolating the self-motion component of the HD system. We developed an (angular) path integration task in whichwe show that rats rely on their internal sense of direction to return to a trial-unique starting location, allowing us to investigate the contribution of the HD system to this behaviour without influences from uncontrolled external cues. Using this path integration task, we show that rats with bilateral lesions of the lateral mammillary nuclei (LMN) are significantly impaired compared to sham-operated controls. Lesions of the LMN, which contains HD cells, are known to abolish directional firing in downstreamHD areas, suggesting that impairment on the task is due to loss of HD activity. We also recorded HD cell activity as rats are performing the path integration task, and found the HD representation to correlate with the rats’ choice of return journey. Thus, we provide both causal and correlational experimental evidence for a critical role of the HD system in path integration. For the second part of this thesis, we implemented a computational model of how the HD system is updated by head movements during path integration, providing a novel explanation for HD cells’ ability to anticipate the animal’s head direction. The model predicts that such anticipatory time intervals (ATIs) should depend on the frequency spectrum of the rats’ headmovements. In direct comparison with experimental recording data, we show that the model can explain up to 80% of the experimentally observed variance, where none was explained by previous models. We also consider the effects of propagating the HD signal through multiple layers, identifying several potential sources of anticipation and lag. In summary, this thesis provides behavioural, lesion, and unit-recording evidence that during path integration, rats use a directional signal provided by the head direction system. The neural mechanisms responsible for the generation and maintenance of this signal are explored computationally. The finding that ATIs depend on the statistics of head movements has methodological implications and constrains models of the HD system.