Abstract
Learning the spatial organization of the environment is essential for most animals' survival. This requires the animal to derive allocentric spatial information from egocentric sensory and motor experience. The neural mechanisms underlying this transformation are mostly unknown. We addressed this problem in electric fish, which can precisely navigate in complete darkness and whose brain circuitry is relatively simple. We conducted the first neural recordings in the preglomerular complex, the thalamic region exclusively connecting the optic tectum with the spatial learning circuits in the dorsolateral pallium. While tectal topographic information was mostly eliminated in preglomerular neurons, the time-intervals between object encounters were precisely encoded. We show that this reliable temporal information, combined with a speed signal, can permit accurate estimation of the distance between encounters, a necessary component of path-integration that enables computing allocentric spatial relations. Our results suggest that similar mechanisms are involved in sequential spatial learning in all vertebrates.
Highlights
Learning to navigate within the spatial organization of different habitats is essential for animals’ survival (Geva-Sagiv et al, 2015)
We characterized the responses of 84 electrosensory PG cells of the weakly electric fish Apteronotus leptorhynchus to moving objects; several motion protocols were used and the sample size for each protocol is mentioned in context (Figure 1—figure supplement 2)
Our results suggest the following space-to-time transformation scheme: PG derives a sequence of discrete novelty events from optic tectum (OT) activity
Summary
Learning to navigate within the spatial organization of different habitats is essential for animals’ survival (Geva-Sagiv et al, 2015). Visual orientation to landmarks and body direction via path integration are combined in the ellipsoid body with dynamics suggestive of a ring attractor While these studies in the simpler nervous system of the fly are closer to providing a mechanistic explanation of how egocentric and external (visual) inputs are combined, it is not clear if the fly has a full representation of the allocentric relations of different environmental features. It is not at all clear that the dynamics of the ellipsoid body can be mapped onto the cortical and hippocampal circuitry of mammals. We hypothesize that egocentric object-related information (OT) conveyed by PG to DL, is converted to a learned allocentric spatial map by the recurrent circuitry of DL, DD and DC; DC, in turn, controls the fish’s spatial behavior via its projections to OT
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