Hippocampal-midbrain circuit enhances the pleasure of anticipation in the prefrontal cortex
Having something to look forward to is a keystone of well-being. Anticipation of a future reward, like an upcoming vacation, can be more gratifying than the experience of reward itself. Theories of anticipation have described how it causes behaviors ranging from beneficial information-seeking to harmful addiction. Here, we investigated how the brain generates and enhances anticipatory pleasure, by analyzing brain activity of human participants who received information predictive of future pleasant outcomes in a decision-making task. Using a computational model of anticipation, we show that three regions orchestrate anticipatory pleasure. We show ventromedial prefrontal cortex (vmPFC) tracks the value of anticipation; dopaminergic midbrain responds to information that enhances anticipation, while the sustained activity in hippocampus provides for functional coupling between these regions. This coordinating role for hippocampus is consistent with its known role in the vivid imagination of future outcomes. Our findings throw new light on the neural underpinnings of how anticipation influences decision-making, while also unifying a range of phenomena associated with risk and time-delay preference.
Additional InformationThe copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. bioRxiv preprint first posted online Mar. 26, 2019. We thank Tim Behrens for his insightful suggestion for the Fourier phase randomization test. We thank Colin Camerer, George Loewenstein, Sandro Romani, Ethan Bromberg-Martin, Jackie Gotlieb, Elliot Ludvig, Yunzhe Liu, Bastian Blain, Giles Story, Laurence Hunt, Jeff Cockburn, Vincent Man, Tomas Aquiono, Caroline Charpentier, Bowen Fung, Wolfgang Pauli, Erin Burkett for the most valuable discussions and helpful suggestions for the manuscript. We also thank radiographers at the UCL for their assistance in running fMRI experiments. This work was supported by the Max Planck Society, the Gatsby Foundation, Wellcome Trust Investigator Award, Japan Society for the Promotion of Science, the Swartz Foundation, Wellcome Sir Henry Dale Fellowship (211155/Z/18/Z), the Jacobs Foundation (2017-1261-04), the Medical Research Foundation, and 2018 NARSAD Young Investigator grant (27023) from the Brain & Behavior Research Foundation.
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