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Research Article

Model-free decision making is prioritized when learning to avoid harming others

View ORCID ProfilePatricia L. Lockwood, View ORCID ProfileMiriam C. Klein-Flügge, Ayat Abdurahman, and Molly J. Crockett
PNAS November 3, 2020 117 (44) 27719-27730; first published October 14, 2020; https://doi.org/10.1073/pnas.2010890117
Patricia L. Lockwood
aDepartment of Experimental Psychology, University of Oxford, Oxford OX1 3PH, United Kingdom;
bWellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX3 9DU, United Kingdom;
cCentre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham B15 2TT, United Kingdom;
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  • ORCID record for Patricia L. Lockwood
  • For correspondence: p.l.lockwood@bham.ac.uk miriam.klein-flugge@psy.ox.ac.uk molly.crockett@yale.edu
Miriam C. Klein-Flügge
aDepartment of Experimental Psychology, University of Oxford, Oxford OX1 3PH, United Kingdom;
bWellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX3 9DU, United Kingdom;
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  • ORCID record for Miriam C. Klein-Flügge
  • For correspondence: p.l.lockwood@bham.ac.uk miriam.klein-flugge@psy.ox.ac.uk molly.crockett@yale.edu
Ayat Abdurahman
aDepartment of Experimental Psychology, University of Oxford, Oxford OX1 3PH, United Kingdom;
bWellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX3 9DU, United Kingdom;
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Molly J. Crockett
aDepartment of Experimental Psychology, University of Oxford, Oxford OX1 3PH, United Kingdom;
dDepartment of Psychology, Yale University, New Haven, CT 06511
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  • For correspondence: p.l.lockwood@bham.ac.uk miriam.klein-flugge@psy.ox.ac.uk molly.crockett@yale.edu
  1. Edited by Fiery Cushman, Harvard University, Cambridge, MA, and accepted by Editorial Board Member Michael S. Gazzaniga September 10, 2020 (received for review May 28, 2020)

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    Fig. 1.

    Model-free and model-based aversive learning task. Participants completed a two-stage decision-making task to assess the tendency to engage in model-free and model-based learning. The task was a hybrid of two tasks previously shown to assess model-free and model-based learning processes (20, 27). We used this task to probe learning to avoid aversive (shock) outcomes for either oneself or another person (the “receiver,” referred to as “other” hereafter). At the beginning of each block, an instruction cue signaled the recipient of the outcome (self or other). At the first stage, two images were displayed that probabilistically led to one of two states (common [∼70% of the time] or uncommon [rare] transition [∼30% of the time]), depicted by different colors surrounding the boxes. In this example, to “blue zone” or “yellow zone” for the other participant and “turquoise zone” or “purple zone” for self. Participants then made a second choice between two pictures in the colored zone which was followed by an outcome of shock or no shock. The probability with which the boxes at the second stage delivered a shock or no-shock outcome drifted throughout the experiment (bounded between 0 and 1 with a drift rate of 0.2) and participants were instructed to keep learning throughout. Ten percent of the total electric shocks accumulated in the “self” condition were delivered to the participant themselves at the end of the experiment, while 10% of the electric shocks accumulated in the “other” condition were delivered to the partner participant.

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    Fig. 2.

    Model-free and model-based choices when avoiding harming oneself and others. (A) Logistic regression coefficients predicting first-level stay/switch choices (mean ± SEM). Participants exhibited a main effect of staying after no pain, which indicated model-free behavior [t(35) = 4.618, P < 0.001, CI for beta estimate: 0.17, 0.42, Cohen’s d = 0.77] and a outcome × transition interaction, which indicated model-based behavior [t(35) = −3.173, P = 0.003, CI for beta estimate: −0.23, −0.05, d = −0.53]. Intriguingly there was also an outcome × recipient interaction [t(35) = −2.31, P = 0.027, CI of beta estimates −0.12, −0.008, d = −0.39] showing that participants were more model-free, and thus more likely to switch after pain and stay after no pain, independent of transition type, when making choices for another person. (B). The probability of repeating a choice at the first level (“stay”) is plotted as a function of the transition and outcome on the previous trial. This shows that the outcome × recipient interaction in A is mostly driven by fewer stay trials after pain, regardless of transition (two rightmost blue vs. orange bars). Thus, the more pronounced model free behavior for others is mostly driven by a lower probability of staying after pain outcomes rather than a higher probability of staying after no pain outcomes). (C) ω estimates from the best-fitting model showed that the ω parameter was significantly lower for other (0.45) than self (0.55), consistent with the regression analyses that showed people were more model-free when avoiding harm to others compared to self (P < 0.02). Asterisks indicate significant difference at P < 0.05.

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    Fig. 3.

    (A and B) Ventral striatum (VS) encodes prediction errors (PE) of pain avoidance for self and other. Ventral striatum (right x = 10, y = 12, z = −4, k = 236, z = 5.84; left x = −16, y = 6, z = −10, k = 458, z = 5.77, P < 0.05 FWE whole brain-corrected after initial thresholding at P < 0.001) tracked model-free prediction errors for both self and other bilaterally, with no significant differences between conditions.

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    Fig. 4.

    Thalamus/caudate signal distinguishes model-free prediction errors for avoiding harm to other vs. self. (A) Thalamus cluster from the contrast other prediction error > self prediction error (x = 16, y = −18, z = 0, k = 84, P = 0.033, Z = 3.50 FWE-SVC from an independent anatomical mask of the thalamus and x = 12 y = −2 z = 4, Z = 4.08, k = 125, P = 0.005 FWE-SVC after initial thresholding at P < 0.001 for a functional ROI derived from Neurosynth to the term “pain” and x = 10 y = −4 z = 4, Z = 3.83, k = 54, and P = 0.002 FWE-SVC for an 8-mm sphere from a meta-analysis of observed pain (68) overlaid on an anatomical scan to show the extent of activation. (B) For illustration, parameter estimates extracted from the thalamus cluster are shown separately for self and other prediction error (PE). See SI Appendix, Fig. S1 for a meta-analysis of neuroimaging studies with the term “pain” that highlights overlapping activation in the thalamus.

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    Fig. 5.

    sgACC tracks stay vs. switch after no pain for other and connects more strongly to dlPFC when switching after no pain for other. (A) sgACC response (x = −2, y = 36, z = 6, K = 498, P = 0.028, FWE whole brain-corrected, after initial thresholding at P < 0.001) to stay vs. switch after no pain for other overlaid on the medial surface of an anatomical scan. The observed BOLD pattern is consistent with model-free behavior (B). Bivariate association between parameter estimates for stay vs. switch after no pain for other in sgACC and greater model-free behavior for other (more negative on x means relatively more model-free for other compared to self). (C) sgACC cluster connects to dlPFC (x = −46, y = 38, z = 26, k = 382, Z = 4.12, P = 0.039, FWE whole brain-corrected after initial thresholding at P < 0.001) during decisions to switch relative to stay after no pain for other. Average slope estimates across participants show stronger connectivity during switch decisions than stay decisions after receiving no pain for other (blue bars) but no difference in sgACC–dlPFC connectivity between stay and switch for self [t(32) = 0.43, P = 0.667, d = 0.08, 95% CI for Cohen’s d = −0.27 0.42; BF01 = 4.92 providing substantial evidence in support of the null] (orange bars). n.s, not statistically significant.

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Model-free decision making is prioritized when learning to avoid harming others
Patricia L. Lockwood, Miriam C. Klein-Flügge, Ayat Abdurahman, Molly J. Crockett
Proceedings of the National Academy of Sciences Nov 2020, 117 (44) 27719-27730; DOI: 10.1073/pnas.2010890117

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Model-free decision making is prioritized when learning to avoid harming others
Patricia L. Lockwood, Miriam C. Klein-Flügge, Ayat Abdurahman, Molly J. Crockett
Proceedings of the National Academy of Sciences Nov 2020, 117 (44) 27719-27730; DOI: 10.1073/pnas.2010890117
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