Hippocampal - gustatory cortical interactions underlying formation of taste-space cognitive maps

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Project Summary/ Abstract Animals need to learn and remember the locations of nourishing and toxic food sources for survival and for adapting to changes in the external environment. It is therefore necessary to associate locations with rewarding and aversive taste experiences in spatial contexts – these are essentially episodic experiences that form associative memories of tastes and spatial locations. It is known that the hippocampus is necessary for episodic memories and formation of spatial cognitive maps, and the gustatory cortex (GC) plays a central role in taste perception as well as for palatability and valence coding. But how networks of neurons in these two regions interact to associate taste palatability information with the spatial contexts in which they occur, and how such interactions drive subsequent behavioral exploration to approach potential food sources, is largely unknown. We have recently discovered a subset of hippocampal CA1 place cells in rats that discriminate tastes based on palatability, providing a foundation for addressing these questions. We found that taste responsive CA1 cells encode taste palatability on a slow timescale in response to taste stimuli, and these taste responses are gated by the spatial responses of individual cells. Further, we also showed that spatial coding of this taste-responsive CA1 sub-network is refined through offline reactivation during sharp-wave ripples (SWRs). Here, we will use a combination of multisite electrophysiology, analyses of behavior, and optogenetic manipulation of inter-regional connectivity to investigate the role of hippocampal-gustatory cortical interactions in forming a spatial cognitive map of ecologically relevant food stimuli. In particular, we hypothesize that networks in CA1 and GC interact for learning, formation, and recall of memories of locations associated with specific taste experiences. We will first use simultaneous recordings from neural ensembles in GC and CA1 regions as rats learn to associate appetitive and aversive tastes with specific locations in an adaptable maze, quantifying how exploration paths change with taste experience. We will investigate the development of taste-location coding in CA1 and the coordination of GC and CA1 activity in service of palatability coding at food source locations. Next, we will test if SWRs in hippocampus at food sources are associated with taste-specific reactivation simultaneously in CA1 and GC, and whether there is coordination of reactivation of taste and location information that can support taste-location associations. Finally, we will use optogenetic perturbation of the input from the taste system to the hippocampus during food sampling to test if this will disrupt formation of discriminative memories for spatial locations of preferred tastes. Together, these aims will provide crucial insight into how networks in the hippocampus interact with primary sensory cortical networks that mediate taste perception, in order to embed ethologically relevant food information in the spatial cognitive map, thus enabling animals to successfully navigate a taste-space cognitive map.