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.
