Interoception drives increased rational decision-making in meditators playing the ultimatum game

Ulrich Kirk, Jonathan Downar, P Read Montague, Ulrich Kirk, Jonathan Downar, P Read Montague

Abstract

Human decision-making is often conceptualized as a competition between cognitive and emotional processes in the brain. Deviations from rational processes are believed to derive from inclusion of emotional factors in decision-making. Here, we investigate whether experienced Buddhist meditators are better equipped to regulate emotional processes compared with controls during economic decision-making in the Ultimatum Game. We show that meditators accept unfair offers on more than half of the trials, whereas controls only accept unfair offers on one-quarter of the trials. By applying fMRI we show that controls recruit the anterior insula during unfair offers. Such responses are powerful predictors of rejecting offers in social interaction. By contrast, meditators display attenuated activity in high-level emotional representations of the anterior insula and increased activity in the low-level interoceptive representations of the posterior insula. In addition we show that a subset of control participants who play rationally (i.e., accepts >85% unfair offers) recruits the dorsolateral prefrontal cortex presumably reflecting increased cognitive demands, whereas rational meditators by contrast display elevated activity in the somatosensory cortex and posterior superior temporal cortex. In summary, when assessing unfairness in the Ultimatum Game, meditators activate a different network of brain areas compared with controls enabling them to uncouple negative emotional reactions from their behavior. These findings highlight the clinically and socially important possibility that sustained training in mindfulness meditation may impact distinct domains of human decision-making.

Keywords: DLPFC; anterior insula; decision-making; fMRI; mindfulness; posterior insula; social fairness; striatum.

Figures

Figure 1
Figure 1
(A) 40 controls and 26 meditators played responders in the Ultimatum Game. Subjects choose on each round to accept or reject a monetary split of $20 made by a new partner on each round. (B) Trial outline for the Ultimatum Game. Each trial started with a jittered fixation period (2–4 s) followed by an offer to split $20 (6 s). Finally subjects indicated the decision to accept or reject the offer (3 s). A red box highlighted the choice being made on each trial. (C) Behavioral results from the Ultimatum Game – meditators (red) displayed significantly higher acceptance rates for the most asymmetric offers from human partners ($19:1 and $18:2) compared to controls (blue). The mean and SEM are plotted.
Figure 2
Figure 2
Within group (A,B) and across group (C,D) main effects of unfair offers. (A) Controls (Ctr) displayed more activity in bilateral superior temporal sulcus (STS), anterior cingulate cortex (ACC), bilateral inferior frontal gyrus (IFG)/anterior insula (AIns), and superior frontal gyrus (MPFC) for unfair offers relative to fair offers by human partners. (B) Significant activity to unfair versus fair offers was found in meditators (Medi) in the thalamus (Thal), bilateral posterior insula (PIns), left mid-anterior insula, and ACC. Direct comparison between unfair offers across groups: (C) Left precuneus (Prc), left dorsal striatum (DStr), and lingual-occipital gyri (LG) are shown overlaid on coronal and sagittal sections. (D) Bilateral mid insula (MIns) and bilateral posterior insula (PIns) are shown on separate coronal sections. The activations are FDR-corrected. The ACC is displayed at p < 0.001, uncorrected to illustrate the extent of the activation.
Figure 3
Figure 3
Meditation-specific activity in posterior insula. (A) Significant interaction effect in meditators compared with controls in response to unfair offers ($19:1–$15:5) relative to fair offers ($10:10–$14:6). Activity was significant in right posterior insula for this contrast. (B) Average beta estimates from 29 voxels in the right posterior insula during the 6-s period following the offer are plotted according to subsequent decision to accept or reject unfair offers ($19:1–$15:5). Activity in this region is driven by unfair offers that are rejected relative to accepted in meditators. In contrast, no such response is significant in controls. (C,D) Average beta estimates from the voxels in the right posterior insula. The plots display a linear scaling with size of unfairness in meditators, which is not present in controls. Mean ± SE are plotted in increments of $2 bins. Activity within the right posterior insula in meditators is significantly correlated with individual differences in trait mindfulness levels as measured by (E) the Mindfulness Attention Awareness Scale (MAAS) and (F) the Kentucky Inventory of Mindfulness Skills (KIMS). The Pearson correlation coefficient (R) is given in the plot. Each data point represents a subject.
Figure 4
Figure 4
ROI analysis in anterior insula. (A) Plots of beta estimates drawn from 5 mm ROIs in left anterior insula based on coordinates from a previous study (Sanfey et al., 2003). Activity within the left anterior insula is plotted against acceptance rates for the most unfair offer sizes ($19:1–$18:2) for each participant separately for (B) controls and (C) meditators. The Pearson correlation coefficient (R) is given in the plot. Each data point in the plot represents a subject. A similar correlation pattern was found for right anterior insula in both groups (not shown). (D) Controls display a significant difference between fair ($10:10–$14:6) and unfair ($19:1–$15:5) offers in the left anterior insula. (E) The meditator group shows no significant differences between fair and unfair responses in the left anterior insula.
Figure 5
Figure 5
Comparison between a subset of participants that play the Ultimatum Game like rational agents; controls (n = 9) and meditators (n = 14). The main effect [Controls > Meditators] display elevated activity in bilateral DLPFC, whereas in the opposite contrast [Meditators > Controls] the left postcentral gyrus (PCG) and left posterior superior temporal cortex (pSTC) are displayed.

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