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Mindfulness meditation modulates reward prediction errors in a passive conditioning task.

Kirk U, Montague PR - Front Psychol (2015)

Bottom Line: Self-control strategies such as those practiced in mindfulness-based approaches is claimed to reduce negative and positive reactions to stimuli suggesting the hypothesis that such training may influence basic reward processing.We found diminished positive and negative PE-related blood-oxygen level-dependent (BOLD) responses in the putamen in meditators compared with controls.In the meditator group this decrease in striatal BOLD responses to reward PE was paralleled by increased activity in posterior insula, a primary interoceptive region.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Southern Denmark Odense, Denmark.

ABSTRACT
Reinforcement learning models have demonstrated that phasic activity of dopamine neurons during reward expectation encodes information about the predictability of reward and cues that predict reward. Self-control strategies such as those practiced in mindfulness-based approaches is claimed to reduce negative and positive reactions to stimuli suggesting the hypothesis that such training may influence basic reward processing. Using a passive conditioning task and fMRI in a group of experienced mindfulness meditators and age-matched controls, we tested the hypothesis that mindfulness meditation influence reward and reward prediction error (PE) signals. We found diminished positive and negative PE-related blood-oxygen level-dependent (BOLD) responses in the putamen in meditators compared with controls. In the meditator group this decrease in striatal BOLD responses to reward PE was paralleled by increased activity in posterior insula, a primary interoceptive region. Critically, responses in the putamen during early trials of the conditioning procedure (run 1) were elevated in both meditators and controls. Overall, these results provide evidence that experienced mindfulness meditators are able to attenuate reward prediction signals to valenced stimuli, which may be related to interoceptive processes encoded in the posterior insula.

No MeSH data available.


Related in: MedlinePlus

Task outline and positive PE signals.(A) Outline of the conditioning task. fMRI scanning consisted of four separate sessions/runs. Catch events were interspersed among the normal events in run 3 and run 4. Run 1 and run 2 consisted on normal (training) trials only. (B) Normal events consisted of a yellow light (1 s) predicting the oral delivery of fruit juice (0.8 ml) 6 s later. Catch events designed to capture a positive reward PE consisted of presentation of the light cue (1 s) and juice delivery 10 s later at an unexpected time. The specific contrast designed to capture the positive PE was: [Juice delivered (unexpected) > Juice delivered (expected)]. (C) Left panel, positive PE for controls display activity in bilateral putamen. Right panel, positive PEs in meditators did not yield significant voxels in the putamen (see Table 1 for complete list of activations). (D) Left panel, group differences to positive reward PEs show SVC-corrected activity in left putamen in controls. Right panel, parameter estimates for the significant voxels in left putamen show an increase in the BOLD signal at times when juice was not expected but delivered. Controls shown in blue and meditators in red. Error bars indicate SE.
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Figure 1: Task outline and positive PE signals.(A) Outline of the conditioning task. fMRI scanning consisted of four separate sessions/runs. Catch events were interspersed among the normal events in run 3 and run 4. Run 1 and run 2 consisted on normal (training) trials only. (B) Normal events consisted of a yellow light (1 s) predicting the oral delivery of fruit juice (0.8 ml) 6 s later. Catch events designed to capture a positive reward PE consisted of presentation of the light cue (1 s) and juice delivery 10 s later at an unexpected time. The specific contrast designed to capture the positive PE was: [Juice delivered (unexpected) > Juice delivered (expected)]. (C) Left panel, positive PE for controls display activity in bilateral putamen. Right panel, positive PEs in meditators did not yield significant voxels in the putamen (see Table 1 for complete list of activations). (D) Left panel, group differences to positive reward PEs show SVC-corrected activity in left putamen in controls. Right panel, parameter estimates for the significant voxels in left putamen show an increase in the BOLD signal at times when juice was not expected but delivered. Controls shown in blue and meditators in red. Error bars indicate SE.

Mentions: To test our experimental predictions, we recruited 58 participants (30 controls and 28 Buddhist meditators) and used a classical conditioning procedure that has been previously used to study reward prediction and cues that predict reward (McClure et al., 2003; Salas et al., 2010). Specifically, participants were presented with a yellow light cue (1 s), which predicted the time of reward delivery (juice). Training consisted of reliably pairing a light cue (presented centrally in participants’ visual field) with oral juice delivery 6 s later. After 45 of such normal events divided into two runs (run 1 = 23 events; run 2 = 22 events), 6 catch events were introduced in run 3 and another 6 catch events in run 4, randomly spaced in between 12 normal events. In the catch events, juice delivery was delayed 4 s beyond the time expected from training events (Figure 1A). Throughout the conditioning procedure juice delivery remained constant (0.8 ml). This conditioning procedure is known to generate two types of PEs during catch events: (1) no juice delivery at expected times generates a negative PE (less than expected), and (2) juice delivery at an unexpected times generates a positive PE (more than expected).


Mindfulness meditation modulates reward prediction errors in a passive conditioning task.

Kirk U, Montague PR - Front Psychol (2015)

Task outline and positive PE signals.(A) Outline of the conditioning task. fMRI scanning consisted of four separate sessions/runs. Catch events were interspersed among the normal events in run 3 and run 4. Run 1 and run 2 consisted on normal (training) trials only. (B) Normal events consisted of a yellow light (1 s) predicting the oral delivery of fruit juice (0.8 ml) 6 s later. Catch events designed to capture a positive reward PE consisted of presentation of the light cue (1 s) and juice delivery 10 s later at an unexpected time. The specific contrast designed to capture the positive PE was: [Juice delivered (unexpected) > Juice delivered (expected)]. (C) Left panel, positive PE for controls display activity in bilateral putamen. Right panel, positive PEs in meditators did not yield significant voxels in the putamen (see Table 1 for complete list of activations). (D) Left panel, group differences to positive reward PEs show SVC-corrected activity in left putamen in controls. Right panel, parameter estimates for the significant voxels in left putamen show an increase in the BOLD signal at times when juice was not expected but delivered. Controls shown in blue and meditators in red. Error bars indicate SE.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4325661&req=5

Figure 1: Task outline and positive PE signals.(A) Outline of the conditioning task. fMRI scanning consisted of four separate sessions/runs. Catch events were interspersed among the normal events in run 3 and run 4. Run 1 and run 2 consisted on normal (training) trials only. (B) Normal events consisted of a yellow light (1 s) predicting the oral delivery of fruit juice (0.8 ml) 6 s later. Catch events designed to capture a positive reward PE consisted of presentation of the light cue (1 s) and juice delivery 10 s later at an unexpected time. The specific contrast designed to capture the positive PE was: [Juice delivered (unexpected) > Juice delivered (expected)]. (C) Left panel, positive PE for controls display activity in bilateral putamen. Right panel, positive PEs in meditators did not yield significant voxels in the putamen (see Table 1 for complete list of activations). (D) Left panel, group differences to positive reward PEs show SVC-corrected activity in left putamen in controls. Right panel, parameter estimates for the significant voxels in left putamen show an increase in the BOLD signal at times when juice was not expected but delivered. Controls shown in blue and meditators in red. Error bars indicate SE.
Mentions: To test our experimental predictions, we recruited 58 participants (30 controls and 28 Buddhist meditators) and used a classical conditioning procedure that has been previously used to study reward prediction and cues that predict reward (McClure et al., 2003; Salas et al., 2010). Specifically, participants were presented with a yellow light cue (1 s), which predicted the time of reward delivery (juice). Training consisted of reliably pairing a light cue (presented centrally in participants’ visual field) with oral juice delivery 6 s later. After 45 of such normal events divided into two runs (run 1 = 23 events; run 2 = 22 events), 6 catch events were introduced in run 3 and another 6 catch events in run 4, randomly spaced in between 12 normal events. In the catch events, juice delivery was delayed 4 s beyond the time expected from training events (Figure 1A). Throughout the conditioning procedure juice delivery remained constant (0.8 ml). This conditioning procedure is known to generate two types of PEs during catch events: (1) no juice delivery at expected times generates a negative PE (less than expected), and (2) juice delivery at an unexpected times generates a positive PE (more than expected).

Bottom Line: Self-control strategies such as those practiced in mindfulness-based approaches is claimed to reduce negative and positive reactions to stimuli suggesting the hypothesis that such training may influence basic reward processing.We found diminished positive and negative PE-related blood-oxygen level-dependent (BOLD) responses in the putamen in meditators compared with controls.In the meditator group this decrease in striatal BOLD responses to reward PE was paralleled by increased activity in posterior insula, a primary interoceptive region.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Southern Denmark Odense, Denmark.

ABSTRACT
Reinforcement learning models have demonstrated that phasic activity of dopamine neurons during reward expectation encodes information about the predictability of reward and cues that predict reward. Self-control strategies such as those practiced in mindfulness-based approaches is claimed to reduce negative and positive reactions to stimuli suggesting the hypothesis that such training may influence basic reward processing. Using a passive conditioning task and fMRI in a group of experienced mindfulness meditators and age-matched controls, we tested the hypothesis that mindfulness meditation influence reward and reward prediction error (PE) signals. We found diminished positive and negative PE-related blood-oxygen level-dependent (BOLD) responses in the putamen in meditators compared with controls. In the meditator group this decrease in striatal BOLD responses to reward PE was paralleled by increased activity in posterior insula, a primary interoceptive region. Critically, responses in the putamen during early trials of the conditioning procedure (run 1) were elevated in both meditators and controls. Overall, these results provide evidence that experienced mindfulness meditators are able to attenuate reward prediction signals to valenced stimuli, which may be related to interoceptive processes encoded in the posterior insula.

No MeSH data available.


Related in: MedlinePlus