Opponent appetitive-aversive neural processes underlie predictive learning of pain relief
Open accessAbstract
Termination of a painful or unpleasant event can be rewarding. However, whether the brain treats relief in a similar way as it treats natural reward is unclear, and the neural processes that underlie its representation as a motivational goal remain poorly understood. We used fMRI (functional magnetic resonance imaging) to investigate how humans learn to generate expectations of pain relief. Using a pavlovian conditioning procedure, we show that subjects experiencing prolonged experimentally induced pain can be conditioned to predict pain relief. This proceeds in a manner consistent with contemporary reward-learning theory (average reward/loss reinforcement learning), reflected by neural activity in the amygdala and midbrain. Furthermore, these reward-like learning signals are mirrored by opposite aversion-like signals in lateral orbitofrontal cortex and anterior cingulate cortex. This dual coding has parallels to 'opponent process' theories in psychology and promotes a formal account of prediction and expectation during pain.
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Relaxation, anxiety, pleasant body sensations, and desire for opioids were measured via validated single items rated on a numeric rating scale (0-10).
“Secondary outcomes were measured via validated single items assessing relaxation, 25 anxiety, 22 pleasant body sensations, 26 and desire for opioids, 27 all rated on a numeric rating scale (0 -10) to minimize patient confusion.”
From Randomized Controlled Trial of Brief Mindfulness Training and Hypnotic Suggestion for Acute Pain Relief in the Hospital Setting. (2017) · cites this paper as [26]
The Subjects section (page unavailable) describes a single 0–10 rating of how pleasant participants found cooling-induced pain relief, supporting the citation attached to pleasant body sensations. It does not establish that the item was validated or that it measured pleasant body sensations more generally. The other outcomes have separate citations in the citing sentence. (LLM, conf=0.85)
Experimental — accuracy not yet measuredlOFC represents aversive error-signals.
“These results are in line with findings that lOFC represents aversive error-signals (Seymour et al., 2005).”
From Top-Down Dysregulation—From ADHD to Emotional Instability (2016) · cites this paper as Seymour et al., 2005
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“For instance, the receipt of aversive cues themselves may in fact be ‘rewarding’, converging in the ventral striatum, if replacing a more aversive cue (Seymour et al., 2005).”
- Authors
- Seymour, B., O'Doherty, J. P., Koltzenburg, M., Wiech, K., Frackowiak, R., Friston, K., & Dolan, R.
- Affiliations
- National Hospital for Neurology and Neurosurgery (GB)
- University College London (GB)
- Fondazione Santa Lucia (IT)
- Corresponding author
- Seymour, Ben
- Venue
- Nature Neuroscience
- Published
- 2005-08-21
- Volume
- 8
- Issue
- 9
- Pages
- 1234-1240
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2132473069
- Cited by
- 439
- References
- 59
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 12 · 2023: 13 · 2022: 17 · 2021: 17 · 2020: 46 · 2019: 17 · 2018: 22 · 2017: 28 · 2016: 23 · 2015: 28 · 2014: 22 · 2013: 31 · 2012: 23
- FWCI
- 9.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- Cambridge University Engineering Department Publications Database (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Pain Management and Placebo Effect
- Keywords
- analgesia, classical conditioning, reward learning, aversion, opponent process theory, pain anticipation, amygdala, midbrain, lateral orbitofrontal cortex, anterior cingulate cortex, reinforcement learning
- MeSH terms
- Avoidance Learning, Behavior Therapy, Brain, Capsaicin, Conditioning, Psychological, Female, Humans, Image Processing, Computer-Assisted, Functional Laterality, Magnetic Resonance Imaging, Male, Models, Biological, Oxygen, Pain, Pain Measurement, Reward, Time Factors, Statistics, Nonparametric, Pain Management
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