Maintaining a Cognitive Map in Darkness: The Need to Fuse Boundary Knowledge with Path Integration

Spatial navigation requires the processing of complex, disparate and often ambiguous sensory data. The neurocomputations underpinning this vital ability remain poorly understood. Controversy remains as to whether multimodal sensory information must be combined into a unified representation, consistent with Tolman's “cognitive map”, or whether differential activation of independent navigation modules suffice to explain observed navigation behaviour. Here we demonstrate that key neural correlates of spatial navigation in darkness cannot be explained if the path integration system acted independently of boundary (landmark) information. In vivo recordings demonstrate that the rodent head direction (HD) system becomes unstable within three minutes without vision. In contrast, rodents maintain stable place fields and grid fields for over half an hour without vision. Using a simple HD error model, we show analytically that idiothetic path integration (iPI) alone cannot be used to maintain any stable place representation beyond two to three minutes. We then use a measure of place stability based on information theoretic principles to prove that featureless boundaries alone cannot be used to improve localization above chance level. Having shown that neither iPI nor boundaries alone are sufficient, we then address the question of whether their combination is sufficient and – we conjecture – necessary to maintain place stability for prolonged periods without vision. We addressed this question in simulations and robot experiments using a navigation model comprising of a particle filter and boundary map. The model replicates published experimental results on place field and grid field stability without vision, and makes testable predictions including place field splitting and grid field rescaling if the true arena geometry differs from the acquired boundary map. We discuss our findings in light of current theories of animal navigation and neuronal computation, and elaborate on their implications and significance for the design, analysis and interpretation of experiments. Author Summary: Do animals need “cognitive maps“? One of the main difficulties in answering this question is finding a definitive scenario where having and not having a “cognitive map“ result in measurably different outcomes. Many key predictions made by models involving some sort of “cognitive map“ can also be replicated by models without a “cognitive map“. Here we consider published data on rodents navigating in darkness inside homogeneous arenas. The head direction system becomes unstable within three minutes in darkness, yet place and grid cells have been reported to fire in the same locations for thirty minutes or longer. We show firstly that it is theoretically implausible for path integration alone to maintain a stable positional representation beyond three minutes, given a drifting head direction system in darkness. Secondly, we prove that even assuming perfect boundary knowledge is insufficient to maintain a stable positional representation. Finally, we show in simulated and real arenas that a nearoptimal combination of path integration and boundary representation is sufficient to produce stable positional representations in darkness consistent with published data. The necessity for fusing path integration and landmark information for accurate localization in darkness is both consistent with, and motivates the existence of, “cognitive maps.“