Abstract

Activity changes in dopaminergic neurons encode the ongoing discrepancy between expected and actual value of a stimulus, providing a teaching signal for a reward prediction process. Previous work comparing a cohort of long-term Zen meditators to controls demonstrated an attenuation of reward prediction signals to appetitive reward in the striatum. Using a cross-commodity design encompassing primary- and secondary-reward conditioning experiments, the present study asks the question of whether reward prediction signals are causally altered by mindfulness training in naïve subjects. Volunteers were randomly assigned to 8 weeks of mindfulness training (MT), active control training (CT), or a one-time mindfulness induction group (MI). We observed a decreased response to positive prediction errors in the putamen in the MT group compared to CT using both a primary and a secondary-reward experiment. Furthermore, the posterior insula showed greater activation to primary rewards, independently of their predictability, in the MT group, relative to CT and MI group. These results support the notion that increased attention to the present moment and its interoceptive features - a core component of mindfulness practice - may reduce predictability effects in reward processing, without dampening (in fact, enhancing) the response to the actual delivery of the stimulus.

Highlights

  • The experimental investigation of single-unit recordings in the monkey’s ventral striatum during reinforcement learning[1], has strongly implicated the dopaminergic neurons of the mesolimbic system in coding the discrepancy between expected and actual value of a stimulus, providing a teaching signal for a reward prediction process based on environmental cues[2,3,4]

  • We first focused on the effect of positive prediction error (PE), that is, on the regions displaying a significant change in BOLD response when receiving juice during catch trials, compared to during regular trials, in runs 3–4

  • Previous work from our group has revealed an association of meditative practice and brain responses with reward prediction errors in a simple conditioning task[12]; because of its cross-cohort design, that study was unable to address the causal impact of mindfulness training (MT) directly

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Summary

Introduction

The experimental investigation of single-unit recordings in the monkey’s ventral striatum during reinforcement learning[1], has strongly implicated the dopaminergic neurons of the mesolimbic system in coding the discrepancy between expected and actual value of a stimulus, providing a teaching signal for a reward prediction process based on environmental cues[2,3,4]. While the role of dopaminergic transmission appears crucial for the successful exploration of the environment in pursuit of rewarding stimuli, the reward system can be maladaptive and promote vulnerability to addiction[7,8,9] In the latter case, where the expected sensations associated with the reward represent the primary causal factor for consumption and for relapse during abstinence, it is important to understand whether specific behaviors or behavioral interventions may be able to attenuate such stimulus-evoked responses. In this perspective, it has been demonstrated[10] that a cognitive strategy of emotion regulation, in the context of a monetary-reward conditioning task, decreased the cue-triggered activation of the striatum associated with reward expectation. In the secondary-reward experiment, we employed a complete randomized longitudinal design where subjects were scanned using fMRI both pre and post intervention

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