Reorganization and reactivation of a preexisting taste-responsive hippocampal network

Summary Animals need to remember the locations of nourishing and toxic food sources for survival, a fact that necessitates a mechanism for associating taste experiences with particular places. We have previously identified such responses within hippocampal place cells [1], the activity of which is thought to aid memory-guided behavior by forming a mental map of an animal’s environment that can be reshaped through experience [2-7]. It remains unknown, however, whether specific place cells are preconfigured to respond to tastes, or whether taste-responsiveness emerges as a result of experience that reorganizes spatial maps. Here, we recorded from neurons in the dorsal CA1 hippocampal region of rats running for taste rewards delivered via intra-oral cannulae at specific locations on a linear track. We found that taste responsiveness was inherent to a subset of cells that, even prior to taste delivery, had larger place fields than non-taste-responsive cells overlapping with stimulus delivery zones. Taste-responsive cells’ place fields then contracted, as a result of taste exposure, to be more restricted to stimulus delivery zones, leading to a stronger representation of rewarded areas on the track. These remapped units exhibited increased sharp-wave ripple co-activation during the taste delivery session, which correlated with the degree of place field contraction. Our results suggest that taste responsivity is preconfigured in a subset of hippocampal place cells, whose spatial representations are then refined by sensory experience to signal reward. This represents a possible mechanism by which animals identify and remember locations where ecologically relevant stimuli are found within their environment.