The Neural Basis of Aversive Pavlovian Guidance during Planning

Níall Lally, Quentin J M Huys, Neir Eshel, Paul Faulkner, Peter Dayan, Jonathan P Roiser

Research output: Contribution to journalArticlepeer-review

110 Downloads (Pure)

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 multistep decisions. Therefore, humans frequently use 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 was associated with the responses of insula and dorsolateral prefrontal cortices to the receipt of large monetary losses, and also with subclinical levels of anxiety. In summary, our data reveal the neural signatures of an important reflexive Pavlovian process that shapes goal-directed evaluations and thereby determines the outcome of high-level sequential cognitive processes.SIGNIFICANCE STATEMENT Multistep 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 subclinical anxiety levels and insular cortex activation. 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.

© 2017, The Authors. The attacheddocument (embargoed until 18/04/2018) is an author produced version of a paperpublished in JOURNAL OF NEUROSCIENCE uploaded in accordance with the publisher’s self-archiving policy. The final published version (version of record) is availableonline at the link below. Some minor differences between this version and thefinal published version may remain. We suggest you refer to the final publishedversion should you wish to cite from it.

Original languageEnglish
Pages (from-to)10215-10229
JournalJOURNAL OF NEUROSCIENCE
Volume37
Issue number42
DOIs
Publication statusPublished - 18 Oct 2017

Keywords

  • Adult
  • Avoidance Learning
  • Choice Behavior
  • Conditioning, Classical
  • Decision Making
  • Female
  • Goals
  • Gyrus Cinguli
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Reaction Time
  • Young Adult
  • Journal Article

Cite this