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/lp/pubmed-central/amygdala-involvement-in-self-blame-regret-RXoIeMWzMo
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- Pubmed Central
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- © 2010 Psychology Press
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- 1747-0919
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- 1747-0927
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- 10.1080/17470919.2010.506128
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Abstract
SOCIAL NEUROSCIENCE, 2011, 6 (2), 178–189 PSNS AMYGDALA AND SELF-BLAME REGRET Antoinette Nicolle and Dominik R. Bach University College London, London, UK Chris Frith University College London, London, UK, and Aarhus University, Aarhus, Denmark Raymond J. Dolan University College London, London, UK Regret-related brain activity is dependent on free choice, but it is unclear whether this activity is a function of more subtle differences in the degree of responsibility a decision-maker exerts over a regrettable outcome. In this experiment, we show that trial-by-trial subjective ratings of regret depend on a higher subjective sense of respon- sibility, as well as being dependent on objective responsibility. Using fMRI we show an enhanced amygdala response to regret-related outcomes when these outcomes are associated with high, as compared to low, responsibility. This enhanced response was maximal in participants who showed a greater level of enhancement in their subjec- tive ratings of regret engendered by an objective increase in responsibility. Orbitofrontal and cingulate cortex showed opposite effects, with an enhanced response for regret-related outcomes when participants were not objectively responsible. The findings indicate that the way the brain processes regret-related outcomes depends on both objective and subjective aspects of responsibility, highlighting the critical importance of the amygdala. Keywords: Counterfactual thinking; Regret; Responsibility; Decision-making; Amygdala. to have acted differently, whereas disappointment is INTRODUCTION associated more with a sense of bad luck and/or power- Liberty means responsibility. That is why most men lessness (Zeelenberg et al., 1998b). While it has been dread it. (George Bernard Shaw, 1856–1950) suggested that outcome regret can be experienced without a feeling of self-blame (Connolly & Zeelenberg, Good or bad events in our lives can invite a comparison 2002; Simonson, 1992), the dominant view is that to what might have been, a psychological process self-blame or responsibility is a necessary prerequisite referred to as “counterfactual thinking.” Outcomes in the experience of regret (see Connolly, Ordónez, & that could have been better from the same choice tend Coughlan, 1997; Ordonez & Connolly, 2000; and to induce feelings of disappointment, while outcomes Zeelenberg, van Dijk, & Manstead, 1998a, 2000 for a that could have been better from a different choice thorough review and discussion). induce feelings of regret (Roese & Olson, 1995). A Neurobiological studies provide compelling evid- focus on this different choice, or a between-option ence for a role of the orbitofrontal cortex (OFC) in counterfactual comparison, invokes the idea that regret. Patients with orbitofrontal cortex lesions do regret depends on reproach, self-blame, and a desire not experience regret but show no impairment in Correspondence should be addressed to: Antoinette Nicolle, Wellcome Trust Centre for Neuroimaging, 12 Queen Square, London WC1N 3BG, UK. E-mail: a.nicolle@fil.ion.ucl.ac.uk This work was supported by a Wellcome Trust Programme Grant to RJD and a Brain Research Trust Prize Studentship to AN. We wish to acknowledge the constructive comments of Jean Decety and two anonymous reviewers on an earlier version of this manuscript. © 2010 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business www.psypress.com/socialneuroscience DOI: 10.1080/17470919.2010.506128 AMYGDALA AND SELF-BLAME REGRET 179 experiencing disappointment (Camille et al., 2004). implicated in agency and motor control, including the Using functional magnetic resonance imaging (fMRI), insula and angular gyrus (Farrer & Frith, 2002; Farrer Coricelli et al. (2005) reported activity in medial OFC et al., 2003), although such regions are implicated associated with the experience of regretful outcomes more in being responsible, as opposed to feeling as well as amygdala activity associated with a ten- responsible. In relation to our central question we dency to avoid choices that might engender regret. predicted regret-related brain activity to be modu- Others report a greater role of the OFC in regret com- lated by the degree to which the outcome of the pared to disappointment (Chua, Gonzalez, Taylor, played gamble is worse than that of the unplayed Welsh, & Liberzon, 2009), regret compared to relief gamble in regions previously implicated in regret (Chandrasekhar, Capra, Moore, Noussair, & Berns, (including OFC, amygdala, hippocampus, ACC, 2008), relative compared to absolute loss (Fujiwara, insula, and striatum), but only with higher levels of Tobler, Taira, Iijima, & Tsutsui, 2008), and evaluat- responsibility. ing incorrect compared to correct choices (Lui et al., 2007). The role of agency in modulating brain activity METHODS associated with choice outcomes has been highlighted by findings that ventral striatal responses to absolute Participants losses and gains depend on agency over the causal choice (Coricelli et al., 2005). We extended this finding We recruited 18 participants (10 female) for the to show that ventral striatal responses to outcomes experiment. All were right-handed with normal or that are relatively better or worse than what might corrected vision, and no history of neurological have been from commitment to a different choice also or psychiatric disorder. Participants’ ages ranged depend on agency (Nicolle, Bach, Driver, & Dolan, in between 19 and 30 years (mean = 23.67 years) and press). However, self-blame regret involves more each gave informed consent, according to procedures than just agency over a choice, depending also on approved by the UCL Research Ethics Committee. social norms and decision justifiability (Connolly & Due to incomplete behavioral data collection, one Zeelenberg, 2002). For example, it is likely to be the participant was removed from the behavioral analysis, case that we can more easily justify a bad decision, but included in the imaging analysis. A second partic- thus reducing feelings of self-blame, if we know oth- ipant was removed from the imaging analysis due to ers would have made a similar choice. Moreover, if scanner malfunction, but was included in the behavioral others actually played a part in the bad decision, self- analysis. A further participant was excluded as blame regret can be reduced by transferring a compo- an outlier, after showing a relationship between nent of responsibility onto them. The likely import- regret-related outcomes and subjective ratings of ance of self-blame in regret led us to predict that regret that was 2.5 standard deviations from the mean regret-related responses would be modulated by the and negative. degree to which a decision-maker feels responsible for an outcome. Thus, we designed an experiment where participants experienced outcomes of “played” Experimental procedure and “unplayed” gambles under various levels of responsibility (a task modified from a design of Mel- Our central aim was to explore how subjective and lers, Schwartz, & Ritov, 1999). While the act of mak- neuronal responses to regret-related outcomes are ing a choice between two gambles was constant modulated by responsibility. We used a task based on across all trials, our paradigm created situations where that of Mellers et al. (1999). In brief, participants were participants’ actual experienced sense of responsibil- instructed to choose between two “wheel-of-fortune” ity for outcomes was systematically varied. The latter gambles on each trial, each incorporating a win and manipulation was realized by informing participants loss outcome with differing probabilities (25%, 50%, that each of their played gambles would depend on or 75%). We used 24 different gamble pairs, allowing their own choice along with the votes of varying num- for four different pairs per probability combination bers of additional individuals. Here, we predicted that (e.g., 25% win against 50% win). Points allocated to participants’ subjective sense of responsibility for the possible winning and loosing outcomes were such gamble outcomes would decrease as a function of that the two gambles in the pair were of equal greater numbers of these “other voters.” expected value (EV) (i.e., probability of win × magni- There are good grounds to expect an effect tude of possible win). In order to enhance feelings of of responsibility being expressed in brain regions skill in the game, two further pair types made up 7% 180 NICOLLE ET AL. of trials and included one gamble of a clearly higher a 2 s delay, participants were then shown the points EV than the other. Details of the gamble pairs used outcome of both the played and the unplayed gamble. are given in Table 1. The outcome of played gamble, whether congruent or An exemplar trial timeline is shown in Figure 1. incongruent with their own gamble choice, deter- Participants were told that their choice would count as mined payment for the experiment. If the played gamble one vote towards the gamble to be played. In mini- was incongruent with the participant’s own gamble blocks of five trials, participants were informed that choice the lowest level of responsibility was pre- they were playing in a group alongside 0, 2, 4, 6, or 8 dicted, as participants were not agents of the choice. If other voters, whom they believed to have performed the played gamble was congruent with the partici- the task in advance, but who were not real. After they pant’s own gamble choice, however, we predicted selected their preferred gamble, the gamble receiving that participants’ subjective sense of responsibility for the highest number of votes from the group (including gamble outcomes would decrease as a function of the their own vote) was played. With more than 0 other increased numbers of “other voters,” even though par- voters, there was a chance that the played gamble ticipants were still the agents of the choice. Partici- would not be congruent with the participant’s own pants received 50p for each percentage they won of choice. The probability of participants’ chosen gamble the maximum points they could have won in their being played varied probabilistically as a function of game. This encouraged participants to compare the the number of voters, such that a greater number of received outcome with what might have been under voters meant an increased chance that their gamble the unplayed gamble, on a trial-by-trial basis. Partici- would not be selected, while in situations of 0 other pants were assumed to treat all trials as having an voters their chosen gamble was always played. After equal impact on their financial gain. TABLE 1 Details of the gamble pairs used in the task, including the probabilities of each of the winning and losing outcomes (in points) of each gamble option Gamble 1 Gamble 2 Outcome 1 Probability 1 Outcome 2 Probability 2 Outcome 1 Probability 1 Outcome 2 Probability 2 180 0.5 −80 0.5 60 0.25 −20 0.75 210 0.5 −20 0.5 130 0.25 −50 0.75 370 0.5 −170 0.5 20 0.5 −120 0.5 430 0.5 −50 0.5 10 0.5 −30 0.5 550 0.5 −30 0.5 80 0.5 −60 0.5 6150 0.5 −10 0.5 190 0.5 −50 0.5 7160 0.5 −80 0.5 60 0.75 −20 0.25 840 0.5 −80 0.5 20 0.75 −140 0.25 970 0.5 −50 0.5 20 0.75 −20 0.25 10 200 0.5 −30 0.5 130 0.75 −50 0.25 11 50 0.5 −30 0.5 80 0.75 −200 0.25 12 50 0.5 −30 0.5 40 0.75 −80 0.25 13 120 0.25 −60 0.75 60 0.25 −40 0.75 14 10 0.25 −50 0.75 40 0.25 −60 0.75 15 100 0.25 −80 0.75 20 0.75 −200 0.25 16 80 0.25 −40 0.75 20 0.75 −100 0.25 17 140 0.25 −30 0.75 20 0.75 −50.25 18 20 0.75 −100 0.25 110 0.25 −50 0.75 19 60 0.75 −60 0.25 150 0.25 −10 0.75 20 60 0.75 −20 0.25 200 0.25 −10 0.75 21 100 0.75 −140 0.25 60 0.75 −20 0.25 22 100 0.75 −80 0.25 80 0.75 −20 0.25 23 10 0.75 −70 0.25 40 0.75 −160 0.25 24 80 0.75 −40 0.25 100 0.75 −100 0.25 25 150 0.5 0 0.5 0 0.5 −50 0.5 26 10 0.5 −200 0.5 200 0.75 −10 0.25 Gamble pairs 1–24 have equal expected value, i.e. (outcome 1 × probability 1) + (outcome 2 × probability 2). Gamble pairs 25 and 26 are catch trials with noticeably different expected values. AMYGDALA AND SELF-BLAME REGRET 181 Figure 1. An exemplar trial timeline. Trials included a choice phase in which participants select their choice of gamble, with choice indicated by a blue box. For each gamble, outcome probabilities were indicated by wedge size, with corresponding outcomes written above in number of points. Number of other voters was also shown, but was constant for mini-blocks of 5 trials. A gamble selection stage followed, in which the gamble receiving the highest number of votes was indicated with a yellow box. This gamble was then played, with its outcome affecting participants’ winnings whether chosen by them or not. Next, the outcome of both the played and the unplayed gambles was revealed. Participants performed both a behavioral session standard automatic 3D-shim procedure was per- and a scanning session, occurring on separate days formed at the beginning of each experiment. Partici- (order counterbalanced across participants). In the pants were scanned with a single-shot gradient-echo behavioral session, participants played 320 trials in planar imaging (EPI) sequence optimized to reduce four games and, after every trial, provided two subjec- blood-oxygen-level-dependent (BOLD) sensitivity tive ratings on a 100-point horizontal visual analog losses in the orbitofrontal cortex due to susceptibility scale (this was not practical in the scanning session). artifacts, using a combination of increased spatial res- The starting position of the slider on each rating scale olution in the readout direction and reduced echo time was random between the extremes of 1 and 100, in (Weiskopf et al., 2007). Imaging parameters were as order to avoid anchoring effects. The rating questions follows: 48 oblique transverse slices tilted by 30°, res- comprised either a memory probe asking “How much olution of 1.5 mm in the readout direction and 3 mm bigger or smaller was the received gamble outcome in the PE direction, slice thickness = 2 mm, gap than what might have been received from the between slices = 1 mm, repetition time TR = 3.12 s, unplayed gamble?” or a rating of subjective feeling α = 90°, echo time TE = 25 ms, bandwidth (BW) = comprising the following probes, “How positive or 1953 Hz/pixel, phase-encoding (PE) direction ante- negative do you feel about the trial outcome?”, “How rior–posterior, field of view (FOV) = 192 × 192 mm , much regret do you feel for outcome?”, and “How matrix size 128 × 64, z-shim gradient pre-pulse responsible do you feel for the outcome?” It was ran- moment = −1.4 mT/m × ms. EPI magnitude images domly decided which two of these four ratings would were reconstructed from the complex k-space raw be presented on each trial. We explained to partici- data using a generalized reconstruction method based pants that these ratings related to their response to the on the measured EPI k-space trajectory to minimize outcome of each trial. Only the memory test, and not ghosting (Josephs, Deichmann, & Turner, 2000). EPI the other ratings, was used during the scanning ses- data acquisition was monitored online using a real- sion (in 10% of trials) in order to enhance the ten- time reconstruction and quality assurance system dency to think counterfactually. In the scanning (Weiskopf et al., 2007). We acquired fieldmaps for session, participants also played 320 trials in four each subject at the start of scanning (Siemens stand- 8-min games. ard double echo gradient echo fieldmap sequence, echo time = 12.46 ms, TR = 10.2 ms, matrix size = 64 × 64, 64 slices covering the whole head, voxel size = 3 × Imaging acquisition 3 × 3 mm). These allowed for calculation of static geometric distortions caused by susceptibility- We scanned participants in a 3 T Allegra scanner induced field inhomogeneities, which were used to (Siemens, Erlangen, Germany) operated with its stand- correct EPI images for both these static distortions ard head transmit–receive coil. The manufacturer’s and any changes in these distortions due to head 182 NICOLLE ET AL. motion (Andersson, Hutton, Ashburner, Turner, & (i.e., only for those outcomes objectively thought to Friston, 2001; Hutton et al., 2002). We also recorded induce regret, rather than relief). heart rate with a pulse oximeter, along with respira- As we obtained multiple subjective ratings from tory phase and volume using a breathing belt. At the each participant along parametric continua of regret, end of the scanning session, we acquired a T1- responsibility and negative feeling, these ratings were weighted anatomical scan for each participant using a standardized for each participant, to avoid anchoring modified driven equilibrium Fourier transform effects, and the standardized regression coefficients (MDEFT) sequence (Ugurbil et al., 1993), with opti- for all analyses were calculated on an individual sub- mized parameters as described in the literature (Deich- ject basis. We report mean standardized regression mann, Schwarzbauer, and Turner, 2004): for each coefficients from the between-subjects level of a hier- volunteer, 176 sagittal partitions were acquired with an achical linear model. Finally, with a one-sample t-test, image matrix of 256 × 224 (Read × Phase). we tested whether participants’ answers on the post- trial memory tests showed performance significantly above chance. This enabled us to verify whether par- Analysis of subjective ratings ticipants were taking into account both the outcomes received from the chosen and the alternative outcome We operationalized “regret-related outcomes” as of the unchosen gamble on each and every trial. those where the outcome of the played gamble showed a negative discrepancy with (i.e., was worse than) that of the unplayed gamble. Our design incor- Imaging processing and analysis porated a continuous variable of this between-gamble negative outcome discrepancy (i.e., received outcome – For fMRI, we used a two-variable parametric design, foregone outcome). We predicted that subjective with one factor for the number of other voters (0, 2, 4, ratings of regret (as well as negative affect) would be 6, and 8 other voters), comprising our manipulation of enhanced with increasingly negative outcome dis- responsibility, and one factor for level of outcome dis- crepancy. We also predicted that subjective ratings of crepancy, which ranged from −200 to +200 points. responsibility would decrease with increasing number This factor was transformed such that positive num- of other voters. Finally, we predicted that the relation- bers were regret-related (i.e., negative outcome dis- ship between subjective regret and negative outcome crepancy). An additional two-level factor was discrepancy would depend on both subjective and expected to influence sense of responsibility, and objective measures of responsibility. We used linear comprised whether a participant’s choice of gamble regressions to test for continuous relationships was congruent or incongruent with the gamble between outcome discrepancy and subjective ratings selected by the majority vote. of regret and negative affect, since the independent Image preprocessing and data analysis were imple- variables were on a continuous scale. To test the rela- mented using Statistical Parametric Mapping software tionship between subjective responsibility, number of in Matlab2009a (SPM8; Wellcome Trust Centre for voters, and choice congruence we used a repeated- Neuroimaging, Institute of Neurology, UCL). After measures ANOVA. To assess our main hypothesis discarding the first six volumes of each run, to allow that regret depends on choice responsibility, and its for T1 equilibration, EPI images were corrected for degree, we tested a multiple regression model with geometric distortions caused by susceptibility- subjective regret ratings as the dependent variable. induced field inhomogeneities. Fieldmaps were proc- The model entered as independent variables the out- essed for each participant using the FieldMap toolbox come discrepancy (from extreme positive to extreme implemented in SPM8 (Hutton, Deichmann, Turner, negative) along with the interaction of this discrep- & Andersson, 2004). The EPI images were then rea- ancy with a measure of responsibility. For the latter, ligned and unwarped using SPM8 (Andersson et al., we tested three distinct measures of responsibility 2001). Each participant’s structural image was coreg- comprising subjective ratings of responsibility, choice istered to the mean of the motion-corrected functional congruency, and the number of other voters. For images using a 12-parameter affine transformation, descriptive purposes, we also performed an ANOVA, and was segmented according to the standard proce- similar to that described above in the case of subjec- dure in SPM8 (Ashburner & Friston, 2005). The spa- tive responsibility, to test the relationship between tial normalization parameters resulting from the subjective regret and number of voters and choice previous step were then applied to the functional congruence for negatively discrepant outcomes only images to allow for intersubject analysis, and finally AMYGDALA AND SELF-BLAME REGRET 183 these images were smoothed using an 8 mm full hippocampus, insula, and ventral and dorsal striatum width, half maximum (FWHM) Gaussian kernel. (all defined anatomically and bilaterally through the For each participant, we constructed an event- WFU PickAtlas in SPM; Maldjian, Laurienti, Bur- related general linear model, including 9 regressors dette, & Kraft, 2003; Tzourio-Mazoyer et al., 2002). of interest. These included one regressor for the To address our hypotheses about how responses to onsets of trial outcomes at each level of responsibility, regret-related (i.e., negatively discrepant) outcomes separated out as full responsibility (i.e., 0 other are modulated by responsibility we compared the voters), along with 2, 4, 6, and 8 other voters. Choice response to increasingly negative outcome discrep- trials in which there were more than 0 other voters ancy under full responsibility (i.e., 0 other voters) were further segregated as a function of whether par- with that when other voters were present. Critically ticipants’ choices were congruent or incongruent, this contrast was performed only on trials where the with the gamble selected by the majority vote. In tri- participant’s own chosen gamble was played (i.e., als with 0 other voters, participants’ choices were congruent choice). Additionally, we compared always congruent with the gamble selected, as partic- response to increasingly negative outcome discrep- ipants were the only voter. Each of these 9 regressors ancy under congruent choice vs. incongruent choice. was parametrically modulated by a mean-corrected We implemented a group-level random-effects ana- regressor of outcome discrepancy. Positive values of lysis using one-sample t-tests on the contrast images this parametric regressor were regret-related out- obtained from each contrast of interest for each partic- comes (i.e., negatively discrepant). Onsets were mod- ipant. Within our regret-related ROIs, we report activ- eled with stick-functions at the time at which ity that survives family-wise error correction for participants received the outcome feedback, con- multiple comparisons at a voxel-level significance of volved with a canonical hemodynamic response p < .05. For completeness, we also report any activity function and its temporal derivative. Motion parame- that survives whole-brain cluster-wise corrected sig- ters defined by the realignment procedure were nificance of p < .05. All reported activity had a voxel- entered as 6 regressors of no interest, along with 17 level uncorrected significance of at least p < .001. additional regressors of cardiac phase (10 regres- sors), respiratory phase (6 regressors) and respiratory volume (1 regressor). Behavioral results We generated statistical parametric maps from contrasts of interest including the main effect of A one-sample t-test confirmed that participants had responsibility as measured by contrasts motivated by above-chance memory for whether the outcome effects of responsibility seen in the subjective ratings received from a played gamble was better or worse results. Here, we were particularly interested in probing than that which might have been received from the activity within the regions of interest (ROIs) reported unplayed gamble, as determined by post-trial memory by Farrer & Frith (2002), as involved in decreased questions, t(15) = 15.09, p < .001, mean percent cor- (the angular gyrus) and increased motor control (the rect = 91.3%. This showed that participants were insula). As mentioned above, while these regions are aware of both the received and the unplayed alternat- implicated in simple motor responsibility (or agency), ive outcomes on each trial. Mean earnings were they may also be involved in processing variations in £12.20 (SD £2.64) in the behavioral session, and blame based on how easily we can assign outcome £22.43 (SD £2.67) in the scanning session. responsibility externally (of key importance for We found a linear effect of number of voters on decision justification models of regret; e.g., Connolly subjective ratings of responsibility, F(1, 15) = 49.5, & Zeelenberg, 2002). Next we tested the main effect p < .001, reflected in an increased sense of responsi- of negative outcome discrepancy (as a linear paramet- bility with decreased number of other voters. The lin- ric effect) where we were interested in activity that ear effect was also significant within congruent increased with greater levels of negative outcome dis- choice trials alone, F(1, 15) = 24.0, p < .001, i.e., crepancy independent of level of responsibility, as when participants had chosen the played gamble, but well as (using a conjunction analysis) brain activity not within incongruent choice trials, F(1, 15) = 0.6, that showed significantly increased response to nega- ns. We also found significant quadratic, F(1, 15) = tive outcome discrepancy across all levels of respon- 9.1, p < .01, and cubic, F(1, 15) = 5.6, p < .05, effects sibility. We tested for these effects within anatomical of voters in the congruent choice condition. Partici- ROIs in regions previously implicated in the experi- pants showed significantly higher ratings of responsi- ence of regret and regret-induced decision bias, including bility for congruent than incongruent choice trials, OFC, anterior cingulate cortex (ACC), amygdala, F(1, 15) = 46.9, p < .001 (Figure 2a, blue line). 184 NICOLLE ET AL. Subjective responsibility (a) (b) Subjective regret 1.5 Congruent choice Incongruent choice 0.8 0.6 0.5 0.4 0.2 –0.5 –1 –0.2 –0.4 –1.5 024682468 low high Subjective responsibility Number of Voters (c) 0.8 0.6 0.4 0.2 –0.2 –0.4 Odiff Odiff x Odiff Odiff x Odiff Odiff x only voters only respon- only congru- sibility ence rating Model 1 Model 2 Model 3 Figure 2. (a) Gradually decreasing mean normalized ratings of subjective responsibility and of subjective regret under congruent and incon- gruent choices with 0, 2, 4, 6, and 8 other voters, otherwise considered objective responsibility. For clarity, subjective regret ratings here are shown only for negatively discrepant outcomes, i.e., where the outcome of the played gamble was worse than the outcome of the unplayed gamble. (b) The mean normalized subjective ratings of regret, displayed as a binary separation of low and high subjective responsibility, for negatively discrepant outcomes. (c) The mean regression coefficients for the three regression models used, each indicating that the predictive value of outcome discrepancy (Odiff) on subjective ratings of regret is greatly enhanced by multiplying this Odiff by one of the three measures of responsibility (number of voters, subjective rating of responsibility, or choice congruence). Error bars show the standard error of the mean across participants. Single-subject standardized regression coefficients, for all three measures of responsibility; namely, taken forward to a between-subject one-sample t-test, decreased number of voters, t(15) = 2.82, p < .02, showed that increasingly negative outcome discrep- increased subjective ratings of responsibility, t(15) = 3.83, ancy significantly predicted greater subjective ratings p < .002, and choice congruency, t(15) = 3.29, of regret, mean R = 0.52, t(15) = 8.04, p < .001. This p < .005. The regression coefficients for the three showed a successful manipulation of subjective regret regression models are illustrated in Figure 2c. These by outcome discrepancy. More negatively discrepant regression models were not restricted to negatively outcomes also significantly predicted increased nega- discrepant outcomes (i.e., they include outcomes tive affect, mean R = 0.71, t(15) = 14.19, p < .001. objectively likely to induce relief, as well as regret), A multiple regression analysis indicated that and were performed using continuous functions of increased responsibility amplified the tendency for subjective responsibility and outcome discrepancy. participants to report high subjective feelings of regret To directly assess the direction of this effect on regret, for outcomes with increasingly negative discrepancy. we show subjective regret for negatively discrepant That is, outcomes were rated as more regretful when outcomes alone under different levels of objective they were both more negative than what would have responsibility, as seen in Figure 2a, and under high been from the alternative gamble and when partici- and low subjective responsibility in Figure 2b. We pants felt more responsible. The three regression found a linear effect of number of voters on subjective models used indicated that this effect was significant ratings of regret for negatively discrepant outcomes, Subjective Rating Regression Coefficient Subjective regret AMYGDALA AND SELF-BLAME REGRET 185 F(1, 15) = 18.7, p < .001, reflected in increased To address whether activity associated with nega- regret with decreased number of other voters. The tive outcome discrepancy is modulated by level of linear effect was significant within congruent choice responsibility, we restricted the analysis to congruent trials alone, F(1, 14) = 6.8, p < .05; i.e., when partic- choice trials, i.e., where the participant’s chosen gam- ipants had chosen the played gamble, but not within ble was played. This was justified on the basis that incongruent choice trials, F(1, 14) = 0.3, ns. Partici- negatively discrepant outcomes received in incongru- pants also showed significantly higher ratings of ent choice trials were associated with participants regret for congruent than incongruent choice trials, actually having been the agents of the post-hoc better F(1, 15) = 30.7, p < .001 (Figure 2a, red line), and choice. Within a priori anatomical ROIs implicated in for high compared to low subjective responsibility, regret, we found no regions showing an entirely linear t(13) = 4.5, p < .001 (Figure 2b). enhanced response to more negatively discrepant out- comes by decreased number of other voters (i.e., increased responsibility). However, in keeping with FMRI results the marked step-like decrease in rated responsibility from 0 to 2 or more other voters (shown in Figure 2a), Manipulation of responsibility we found that left amygdala activity was enhanced for more negatively discrepant outcomes during full We examined the effect of linearly decreasing responsibility trials, and not when there were any responsibility, following the pattern shown in Figure 2a. number of other voters (Figures 3b and 3c) (within While no areas showed a significant effect of increasing anatomically specified bilateral ROI of the amy- responsibility, we found significant corrected level gdala). A linear interaction of outcome discrepancy effects in superior frontal cortex (MNI 51, 26, 31), and responsibility (within congruent choice trials) brainstem (MNI 0, −34, −26) and left insula (−45, 14, was seen in right amygdala activity but only in partic- −8) for decreasing responsibility. In our a priori ROIs, ipants who showed a greater enhancement of subjec- right angular gyrus activity (within a 20 mm sphere tive regret by responsibility (in the form of decreased radius of the coordinates reported by Farrer & Frith, numbers of other voters) in the separate behavioral 2002) significantly increased with decreasing respon- session (Figure 3d), an effect also seen in left amy- sibility (MNI 57, −43, 34), as did bilateral insula gdala at a trend level of significance. (MNI right 30, 20, −11 and left −45, 14, −8). No By contrast, activity in middle cingulate cortex and regions dissociated, at the time of outcome, between angular gyrus showed an increased response to more played gambles that were congruent or incongruent negatively discrepant outcomes, when the played with the participant’s own choice, at a whole-brain gamble was incongruent (whole-brain cluster cor- corrected level. However, right insula activity showed rected p < .05), compared to when it was congruent such an effect within our a priori ROI of bilateral with the participant’s own choice. This indicates a insula (MNI 30, 20, −14). role of middle cingulate cortex and angular gyrus in the processing of regret-related outcomes that are Manipulation of regret externally enforced. Furthermore, activity in middle cingulate cortex, left angular gyrus, and lateral OFC Averaged across all levels of responsibility we responsive to average effect of regret-related out- found significantly increased activity as outcomes comes (Figure 3a) showed a greater response to more became linearly more negatively discrepant in left negatively discrepant outcomes on these incongruent angular gyrus and lateral OFC (Figure 3a). Activity in trials compared to congruent trials (although this was our other a priori ROIs, in the amygdala, hippocampus, only at p < .005 uncorrected level for the lateral ACC, and insula, did not show this effect. Crucially, no OFC). This indicates that regret-related activity in regions showed responsibility-invariant responses to these regions is not associated with self-blame. negatively discrepant outcomes, as evident in a con- junction analysis, providing evidence against a neural representation of a purely outcome-based form of DISCUSSION regret. Instead, regret-related responses in angular gyrus and lateral OFC appeared to be dependent on the In agreement with previous research (e.g., Zeelenberg level of responsibility. However, it is important to note et al., 1998b), we found that subjective ratings of that the reduced power inherent in such a conjunction regret depend both on the outcome being worse than analysis means that we cannot reject the null hypothe- what might have been and on having a sense of sis that such responsibility-invariant responses do exist. responsibility. We now provide new evidence that 186 Figure 3. Group SPM data, thresholded at p < .005 for display purposes, shown on a normalized canonical template brain. (a) Activity in angular gyrus (peak at −42, −64, 25) and lateral OFC (peak at 51, 38, −11) associated with the average effect of linearly increasing negative outcome discrepancy. (b) Enhanced activity in amygdala (peak −18, −1, −20) associated with increasingly negatively out- come discrepancy during full responsibility (0 other voters) compared to other congruent choice trials in the presence of other voters. Plotted in (c) are the beta weights showing the same amygdala response to increasingly negative outcome discrepancy under the different numbers of other voters. (d) Right amygdala activity (peak 30, 5, −26) showing greater enhancement of its response (FWE cor- rected) to more negatively discrepant outcomes by increased responsibility in participants who showed a greater enhancement of subjective regret for increasingly negative outcome discrepancy by increased responsibility (decreased number of voters). Coordinates are in MNI space. Error bars show standard error of the mean. AMYGDALA AND SELF-BLAME REGRET 187 subjective regret depends on the level of subjective actions and their outcomes, which are vital in adapting responsibility even though the individual’s own future behavior. Specifically self-relevant information choice or action directly contributed to the regret- may be passed to the amygdala from other task-engaged related outcome (as in the case of congruent trials). cortical regions (for example, we have shown informa- These findings indicate that regret is not just a func- tion about responsibility and between-option outcome tion of being an agent of a choice but also depends on comparisons to be associated with activity in the angu- subtle changes in sense of responsibility, or accounta- lar gyrus and prefrontal cortex), in order to allocate pro- bility, for the outcomes of our actions. In keeping cessing resources to control mechanisms driving with these behavioral effects we found that regret- adaptive behavior. In keeping with such a framework, related neuronal activity in the amygdala was there is good evidence that the amygdala imparts enhanced by increased responsibility, suggesting a information necessary for acquiring stimulus–reward critical role in “self-blame regret.” This effect was associations to the OFC, which uses this information to magnified in participants who displayed a greater guide behavior (Pickens et al., 2003; Arana et al., 2003; enhancement of their subjective ratings of regret by Schoenbaum, Gottfried, Murray, & Ramus, 2007), responsibility. Interestingly, we did not find any brain allowing for behavioral flexibility in accordance with regions responding to what has been termed “outcome strategic goals (Morris & Dolan, 2004). regret,” i.e., showing invariant responses to regret- The possibility of medial–lateral differences of related outcomes under all levels of responsibility. OFC involvement in regret is worthy of discussion. This suggests that, as for the psychological experience While the null effect in the medial OFC does not chal- of regret, the way the brain processes regretful events lenge the role of medial OFC involvement in the self- may crucially depend on a sense of responsibility. blame component of regret, it is surprising that we The human amygdala is known to be important in find lateral OFC involvement in negatively discrepant emotional memory (Cahill, Babinsky, Markowitsch, outcomes without responsibility. It is possible that this & McGaugh, 1995; Richardson, Strange & Dolan, lateral OFC response reflects anger, frustration, or 2004; Strange & Dolan, 2004) and in learning stimu- loss of control in the participant, on the realization lus–reward associations (e.g., Buechel, Morris, that the other voters contributed to a bad outcome for Dolan, & Friston, 1997; Gottfried, O’Doherty, & the group. On the other hand, it may reflect the partic- Dolan, 2003; LaBar, Gatenby, Gore, LeDoux, & ipant’s rejoicing associated with the knowledge that Phelps, 1998; Whalen et al., 2004). A model of amy- they made the better choice on these incongruent gdala function in our study relates to its putative role trials, despite the received outcome being aversive. as a “relevance detector” (Sander, Grafman, & Zalla, Our finding of strong negative affect associated with 2003; Bach et al., 2008). This proposes that the amy- low responsibility in our task, along with reports that gdala is involved in focusing attentional and physio- lateral OFC processes the unpleasantness of external logical resources towards cues that have special stimuli (e.g., Anderson et al., 2003), support the relevance for personal safety or success. Amygdala former view. It is further possible that any medial activation is found in socially relevant situations, such OFC response associated with self-blame may have as viewing untrustworthy or novel faces (Winston, been overshadowed by more lateral OFC involvement Strange, O’Doherty, & Dolan, 2002; Wright, Martis, in such externally attributed negative emotions. Schwartz, Shin, Fischer, McMullin, et al., 2003) when Understanding the role of subjective responsibility following eye gaze (Kawashima et al., 1999), as well and blame in regret may help in formulating therapies as for especially self-relevant situations, as when for painful and debilitating life regrets. An ability to hearing one’s own name being presented during sleep externally shift responsibility for our bad choices can (Portas et al., 2000). Moreover, the amygdala is impli- reduce feelings of regret (Zeelenberg & Pieters, cated in biasing future decisions based on previous 2007), while understanding that others have made regret (Coricelli et al., 2005), emphasizing its import- similarly bad choices can provide justification for our ance in goal-directed motivation. Regret associated actions by placing us within the social norm with high responsibility is an experience with particu- (Connolly & Zeelenberg, 2002). On the other hand, lar self-relevance, while also providing a strong moti- ability to accept responsibility for our actions can vation for future behavior, such as motivating active motivate adaptive future behaviors, leading to long- attempts to (or intentions to) undo unpleasant events term improvements in quality of life. In real-life (Zeelenberg et al., 1998b; Zeelenberg & Pieters, decision-making, anticipating future regret has positive 1999). On the other hand, a failure to appropriately influences on decisions in sexual behavior (e.g., Richard, accept responsibility for our mistakes may interfere Van der Pligt, & de Vries, 1996), consumer choices with learning accurate associations between our (e.g., Inman & Zeelenberg, 2002; Tsiros & Mittal, 188 NICOLLE ET AL. Connolly, T., Ordónez, L. D., & Coughlan, R. (1997). 2000), and health-related choices (e.g., Lechner, de Regret and responsibility in the evaluation of decision Vries, & Offermans, 1997). Reb (2008) also found outcomes. Organizational Behavior and Human Deci- that anticipating regret can improve the quality of the sion Processes, 70(1), 73–85. decision process by increasing vigilance and careful- Connolly, T., & Zeelenberg, M. (2002). Regret in decision ness. Furthermore, decision-making in areas of busi- making. Current directions in psychological science, 11(6), 212–216. ness, politics, the legal world, health care, and Coricelli, G., Critchley, H. 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Journal
Social Neuroscience – Pubmed Central
Published: Aug 13, 2010