Flexible behavioral adjustment to frustrative nonreward in anticipatory behavior, but not in consummatory behavior, requires the dorsal hippocampus

Abstract

The hippocampus (HC) is recognized for its pivotal role in memory-related plasticity and facilitating adaptive behavioral responses to reward shifts. However, the nature of its involvement in the response to reward downshifts remains to be determined. To bridge this knowledge gap, we explored the HC's function through a series of experiments in various tasks involving reward downshifts and using several neural manipulations in rats. In Experiment 1, complete excitotoxic lesions of the HC impaired choice performance in an 8-maze task after reducing the quantity of sugar pellet rewards. In Experiment 2, whereas chemogenetic inhibition of the dorsal HC left consummatory responses unaffected after a sucrose downshift, it significantly disrupted anticipatory behavior following a food-pellet reward reduction. Experiments 3-5 used peripheral lipopolysaccharide (LPS) treatment and found an increase in cytokine levels in the dorsal HC (dHC, Experiment 3), impaired anticipatory choice (Experiment 4), but no effect on consummatory behavior in two reward-downshift tasks. In Experiment 6, after a sucrose downshift, we found no evidence of increased activation in either the dorsal or ventral HC, as measured by c-Fos expression. These findings highlight the HC's pivotal role in adaptively modulating anticipatory behavior in response to frustrative nonreward, while having no effect on adjustments of consummatory behavior. Spatial orientation, memory update, choice of reward signals of different value, and anticipatory vs. consummatory adjustments to reward downshift are discussed as potential mechanisms that could elucidate the specific effects observed from HC manipulations.