Hippocampal lesions prevent adjustment to reward devaluation
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Incentive relativity refers to a distortion in the absolute value of an incentive that results from the comparison between the present and the memory of past rewards, and it triggers frustration when this comparison indicates that an incentive has been lost. The adaptive value of frustration resides in its ability to cause a rapid change in learning and performance preventing perseveration on no-longer rewarded responses. Thus, frustration facilitates a switch from responses that no longer yield incentives to a search mode that may result in the discovery of needed resources. However, in vulnerable individuals, reward loss can also result in maladaptive persistent behaviors that can lead to neuropsychiatric disorders. A large body of evidence links reward loss experience with aversive emotion (anxiety, disappointment), negative affect (depression), and activation of the hypothalamic-pituitary-adrenal axis (stress). Animal models of frustrative nonreward provide a useful approach to study reward value, and its behavioral consequences from a psychobiological perspective because they enable a careful manipulation of physiological and environmental variables, and a systematic recording of behavioral and neural responses. While little is known about the neural circuit mechanisms of incentive relativity in rodents, there is a good indication that the hippocampus could be involved because (1) reward value needs reward representation, and (2) reward value needs memory, since it is based on reward comparisons. Because women are twice as likely as men to present the disorders that reward loss can induce (Canuto et al., 2018; Kessler & Bromet, 2013), we decided to use female rats for our experiments. Adult female rats with either a hippocampal lesion (n=7) or a sham lesion (n=6) were exposed to a reduction in the amount of expected solid food presented in one of the two goal sites of a figure-eight-maze. Response latencies and choice responses were registered before and after the incentive downshift. We found that excitotoxic lesions of the hippocampus prevented behavioral adjustment to reward devaluation. In particular, unlike control rats, hippocampal lesion rats did not change their preference and perseverated on choosing the downshifted reward, demonstrating a lack of flexibility to modify their response to the new reward conditions. Our results indicate that hippocampal reward computations are required to flexibly guide behavior at the service of obtaining biologically relevant rewards. Identifying the function of neural circuits for reward value and resilience to loss is a critical step for developing therapeutic approaches to prevent or ameliorate emotional and cognitive problems in disease.