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A neurocomputational account of how inflammation enhances sensitivity to punishments versus rewards

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posted on 2023-06-08, 22:27 authored by Neil Harrison, Valerie Voon, Mara Cercignani, Ella A Cooper, Mathias Pessiglione, Hugo CritchleyHugo Critchley
BACKGROUND: Inflammation rapidly impairs mood and cognition and, when severe, can appear indistinguishable from major depression. These sickness responses are characterized by an acute reorientation of motivational state; pleasurable activities are avoided, and sensitivity to negative stimuli is enhanced. However, it remains unclear how these rapid shifts in behavior are mediated within the brain. METHODS: Here, we combined computational modeling of choice behavior, experimentally induced inflammation, and functional brain imaging (functional magnetic resonance imaging) to describe these mechanisms. Using a double-blind, randomized crossover study design, 24 healthy volunteers completed a probabilistic instrumental learning task on two separate occasions, one 3 hours after typhoid vaccination and one 3 hours after saline (placebo) injection. Participants learned to select high probability reward (win £1) and avoid high probability punishment (lose £1) stimuli. An action-value learning algorithm was fit to the observed behavior, then used within functional magnetic resonance imaging analyses to identify neural coding of prediction error signals driving motivational learning. RESULTS: Inflammation acutely biased behavior, enhancing punishment compared with reward sensitivity, through distinct actions on neural representations of reward and punishment prediction errors within the ventral striatum and anterior insula. Consequently, choice options leading to potential rewards were less behaviorally attractive, and those leading to punishments were more aversive. CONCLUSIONS: Our findings demonstrate the neural mediation of a rapid, state-dependent reorientation of reward versus punishment sensitivity during inflammation. This mechanism may aid the adaptive reallocation of metabolic resources during acute sickness but might also account for m

History

Publication status

  • Published

File Version

  • Published version

Journal

Biological Psychiatry

ISSN

0006-3223

Publisher

Elsevier

Issue

1

Volume

80

Page range

73-81

Department affiliated with

  • BSMS Neuroscience Publications

Full text available

  • Yes

Peer reviewed?

  • Yes

Legacy Posted Date

2015-09-10

First Open Access (FOA) Date

2015-09-10

First Compliant Deposit (FCD) Date

2015-09-10

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