Lally, N;
Huys, QJM;
Eshel, N;
Faulkner, P;
Dayan, P;
Roiser, JP;
(2017)
The neural basis of aversive Pavlovian guidance during planning.
Journal of Neuroscience
, 37
(42)
pp. 10215-10229.
10.1523/JNEUROSCI.0085-17.2017.
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Abstract
Important real-world decisions are often arduous as they frequently involve sequences of choices, with initial selections affecting future options. Evaluating every possible combination of choices is computationally intractable, particularly for longer multi-step decisions. Therefore, humans frequently employ heuristics to reduce the complexity of decisions. We recently used a goal-directed planning task to demonstrate the profound behavioral influence and ubiquity of one such shortcut, namely aversive pruning, a reflexive Pavlovian process that involves neglecting parts of the decision space residing beyond salient negative outcomes. However, how the brain implements this important decision heuristic, and what underlies individual differences have hitherto remained unanswered. Therefore, we administered an adapted version of the same planning task to healthy male and female volunteers undergoing functional magnetic resonance imaging (fMRI) to determine the neural basis of aversive pruning. Through both computational and standard categorical fMRI analyses, we show that when planning was influenced by aversive pruning, the subgenual cingulate cortex was robustly recruited. This neural signature was distinct from those associated with general planning and valuation, two fundamental cognitive components elicited by our task but which are complementary to aversive pruning. Furthermore, we found that individual variation in levels of aversive pruning were associated with the responses of insula and dorsolateral prefrontal cortex to the receipt of large monetary losses, and also with sub-clinical levels of anxiety. In summary, our data reveal the neural signatures of an important reflexive Pavlovian processes that shapes goal-directed evaluations, and thereby determines the outcome of high-level sequential cognitive processes.SIGNIFICANCE STATEMENTMulti-step decisions are complex because initial choices constrain future options. Evaluating every path for long decision sequences is often impractical; thus, cognitive shortcuts are often essential. One pervasive and powerful heuristic is aversive pruning, in which potential decision-making avenues are curtailed at immediate negative outcomes. We used neuroimaging to examine how humans implement such pruning. We found it to be associated with activity in the subgenual cingulate cortex, with neural signatures that were distinguishable from those covarying with planning and valuation. Individual variations in aversive pruning levels related to sub-clinical anxiety levels and insular cortex activity. These findings reveal the neural mechanisms by which basic negative Pavlovian influences guide decision-making during planning, with implications for disrupted decision-making in psychiatric disorders.
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