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Striatal structure and function predict individual biases in learning to avoid pain.

ABSTRACT: Pain is an elemental inducer of avoidance. Here, we demonstrate that people differ in how they learn to avoid pain, with some individuals refraining from actions that resulted in painful outcomes, whereas others favor actions that helped prevent pain. These individual biases were best explained by differences in learning from outcome prediction errors and were associated with distinct forms of striatal responses to painful outcomes. Specifically, striatal responses to pain were modulated in a manner consistent with an aversive prediction error in individuals who learned predominantly from pain, whereas in individuals who learned predominantly from success in preventing pain, modulation was consistent with an appetitive prediction error. In contrast, striatal responses to success in preventing pain were consistent with an appetitive prediction error in both groups. Furthermore, variation in striatal structure, encompassing the region where pain prediction errors were expressed, predicted participants' predominant mode of learning, suggesting the observed learning biases may reflect stable individual traits. These results reveal functional and structural neural components underlying individual differences in avoidance learning, which may be important contributors to psychiatric disorders involving pathological harm avoidance behavior.

SUBMITTER: Eldar E

PROVIDER: S-EPMC4855606 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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Striatal structure and function predict individual biases in learning to avoid pain.

Eldar Eran E Hauser Tobias U TU Dayan Peter P Dolan Raymond J RJ

Proceedings of the National Academy of Sciences of the United States of America 20160411 17

Pain is an elemental inducer of avoidance. Here, we demonstrate that people differ in how they learn to avoid pain, with some individuals refraining from actions that resulted in painful outcomes, whereas others favor actions that helped prevent pain. These individual biases were best explained by differences in learning from outcome prediction errors and were associated with distinct forms of striatal responses to painful outcomes. Specifically, striatal responses to pain were modulated in a ma ...[more]

PMID: 27071092

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Project description:BackgroundLearning to predict threatening events enables an organism to engage in protective behavior and prevent harm. Failure to differentiate between cues that truly predict danger and those that do not, however, may lead to indiscriminate fear and avoidance behaviors, which in turn may contribute to disability in people with persistent pain. We aimed to test whether people with persistent neck pain exhibit contingency learning deficits in predicting pain relative to pain-free, gender-and age-matched controls.MethodWe developed a differential predictive learning task with a neck pain-relevant scenario. During the acquisition phase, images displaying two distinct neck positions were presented and participants were asked to predict whether these neck positions would lead to pain in a fictive patient with persistent neck pain (see fictive patient scenario details in Appendix A). After participants gave their pain-expectancy judgment in the hypothetical scenario, the verbal outcome (PAIN or NO PAIN) was shown on the screen. One image (CS+) was followed by the outcome "PAIN", while another image (CS-) was followed by the outcome "NO PAIN". During the generalization phase, novel but related images depicting neck positions along a continuum between the CS+ and CS- images (generalization stimuli; GSs) were introduced to assess the generalization of acquired predictive learning to the novel images; the GSs were always followed by the verbal outcome "NOTES UNREADABLE" to prevent extinction learning. Finally, an extinction phase was included in which all images were followed by "NO PAIN" assessing the persistence of pain-expectancy judgments following disconfirming information.ResultsDifferential pain-expectancy learning was reduced in people with neck pain relative to controls, resulting from patients giving significantly lower pain-expectancy judgments for the CS+, and significantly higher pain-expectancy judgments for the CS-. People with neck pain also demonstrated flatter generalization gradients relative to controls. No differences in extinction were noted.DiscussionThe results support the hypothesis that people with persistent neck pain exhibit reduced differential pain-expectancy learning and flatter generalization gradients, reflecting deficits in predictive learning. Contrary to our hypothesis, no differences in extinction were found. These findings may be relevant to understanding behavioral aspects of chronic pain.

Dataset Information

Striatal structure and function predict individual biases in learning to avoid pain.

Publications

Striatal structure and function predict individual biases in learning to avoid pain.

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