Neural systems underlying aversive conditioning in humans with primary and secondary reinforcers
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Money is a secondary reinforcer commonly used across a range of disciplines in experimental paradigms investigating reward learning and decision-making. The effectiveness of monetary reinforcers during aversive learning and associated neural basis, however, remains a topic of debate. Specifically, it is unclear if the initial acquisition of aversive representations of monetary losses depends on similar neural systems as more traditional aversive conditioning that involves primary reinforcers. This study contrasts the efficacy of a biologically defined primary reinforcer (shock) and a socially defined secondary reinforcer (money) during aversive learning and its associated neural circuitry. During a two-part experiment, participants first played a gambling game where wins and losses were based on performance to gain an experimental bank. Participants were then exposed to two separate aversive conditioning sessions. In one session, a primary reinforcer (mild shock) served as an unconditioned stimulus (US) and was paired with one of two colored squares, the conditioned stimuli (CS+ and CS-, respectively). In another session, a secondary reinforcer (loss of money) served as the US and was paired with one of two different CS. Skin conductance responses were greater for CS+ compared to CS- trials irrespective of type of reinforcer. Neuroimaging results revealed that the striatum, a region typically linked with reward-related processing, was found to be involved in the acquisition of aversive conditioned response irrespective of reinforcer type. In contrast, the amygdala was involved during aversive conditioning with primary reinforcers, as suggested by both an exploratory fMRI analysis and a follow-up case study with a patient with bilateral amygdala damage. Taken together, these results suggest that learning about potential monetary losses may depend on reinforcement learning related systems, rather than on typical structures involved in more biologically based fears.
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The effects of damage to the human amygdala on emotion and emotional experience are much more subtle than the effects of damage to the OFC.
“Although the amygdala has many of the same connections as the OFC (Fig. 2), it is an evolutionarily old brain region, and appears to be overshadowed by the OFC in humans, in that the effects of damage to the human amygdala on emotion and emotional experience are much more subtle (Whalen and Phelps, 2009; Delgado et al., 2011; LeDoux and Pine, 2016; LeDoux et al., 2018) than that of damage to the”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Delgado et al., 2011
The neuroimaging literature is profoundly inconsistent on the role of the striatum in aversive learning, with some studies reporting increased VS activity in aversive contexts and others reporting decreased activity.
“the neuroimaging literature is profoundly inconsistent on this point, with some studies reporting increased VS activity in aversive contexts (Figure 2c) [62–64] and others reporting decreasing activity in this area during the prediction, learning, and receipt of aversive outcomes [65,66].”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [62]
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Challenges of Interpreting Frontal Neurons during Value-Based Decision-Making
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- Authors
- Delgado, M. R., Jou, R. L., & Phelps, E. A.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- New York University (US)
- Corresponding author
- Phelps, Elizabeth A.
- Venue
- Frontiers in Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2011
- Volume
- 5
- Pages
- 71-71
- ISSN
- 1662-453X (ISSN-L)
- 1662-4548
- PMC
- PMC3101377
- OpenAlex
- W2136145111
- Cited by
- 141
- References
- 55
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 8 · 2023: 2 · 2022: 11 · 2021: 21 · 2020: 8 · 2019: 16 · 2018: 15 · 2017: 7 · 2016: 8 · 2015: 6 · 2014: 5 · 2013: 10 · 2012: 10
- FWCI
- 4.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- James S. McDonnell Foundation
- National Institute of Mental Health (R01MH080756)
- National Institute on Drug Abuse (R01DA027764)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- aversive conditioning, primary reinforcers, secondary reinforcers, financial losses, shock, fear conditioning, striatum, amygdala, amygdala damage, reinforcement learning, skin conductance, gambling
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