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Expectation Modulates Neural Responses to Pleasant and Aversive Stimuli in Primate Amygdala
Open accessAbstract
Animals and humans learn to approach and acquire pleasant stimuli and to avoid or defend against aversive ones. However, both pleasant and aversive stimuli can elicit arousal and attention, and their salience or intensity increases when they occur by surprise. Thus, adaptive behavior may require that neural circuits compute both stimulus valence--or value--and intensity. To explore how these computations may be implemented, we examined neural responses in the primate amygdala to unexpected reinforcement during learning. Many amygdala neurons responded differently to reinforcement depending upon whether or not it was expected. In some neurons, this modulation occurred only for rewards or aversive stimuli, but not both. In other neurons, expectation similarly modulated responses to both rewards and punishments. These different neuronal populations may subserve two sorts of processes mediated by the amygdala: those activated by surprising reinforcements of both valences-such as enhanced arousal and attention-and those that are valence-specific, such as fear or reward-seeking behavior.
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“These findings suggest that OT modulates context-specific processing associated with both negative and positive valence in the amygdala, consistent with the encoding of both positive and negative motivational values by the primate amygdala neurons (Belova et al., 2007; Paton et al., 2006).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Belova et al., 2007
In the citing paper
“In addition to being essential for aversively motivated learning, plasticity in the LA is also required for several forms of appetitively motivated learning (43–45) and a number of studies have found that separate populations of amygdala neurons mediate aversive and appetitive processing (46–48).”
From Optical activation of lateral amygdala pyramidal cells instructs associative fear learning (2010) · cites this paper as [48]
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“In monkeys, Belova et al. (2007) have shown that fix-spot responses can be regarded as the earliest predictors of reward.”
BackgroundBoll, S., Gamer, M., Gluth, S., Finsterbusch, J., & Büchel, C. (2012) · European Journal of Neuroscience · doi:10.1111/ejn.12094 · Cited by 98
Reward Magnitude Coding in Primate Amygdala Neurons
Bermúdez, M. A., & Schultz, W. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00540.2010 · Cited by 88
The Dopamine Prediction Error: Contributions to Associative Models of Reward Learning
Nasser, H. M., Calu, D. J., Schoenbaum, G. M., & Sharpe, M. J. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00244 · Cited by 97
Metadata
- Authors
- Belova, M. A., Paton, J. J., Morrison, S. E., & Salzman, C. D.
- Affiliations
- Columbia University (US)
- New York State Psychiatric Institute (US)
- Corresponding author
- Salzman, C. Daniel
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2007-09
- Volume
- 55
- Issue
- 6
- Pages
- 970-984
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2042139
- OpenAlex
- W2133622401
- Cited by
- 349
- References
- 65
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 10 · 2023: 15 · 2022: 11 · 2021: 17 · 2020: 15 · 2019: 18 · 2018: 16 · 2017: 28 · 2016: 17 · 2015: 32 · 2014: 22 · 2013: 23 · 2012: 29
- FWCI
- 10.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2146 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institute on Drug Abuse
- National Eye Institute
- National Science Foundation
- National Institute of Mental Health
- Eunice Kennedy Shriver National Institute of Child Health and Human Development
- 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
- amygdala, expectations, surprise, reinforcement learning, reward, punishment, aversive stimuli, stimulus valence, stimulus intensity, arousal, attention, fear, reward seeking
- MeSH terms
- Amygdala, Animals, Arousal, Data Interpretation, Statistical, Learning, Macaca mulatta, Neurons, Psychomotor Performance, Reinforcement, Psychology, ROC Curve, Excitatory Postsynaptic Potentials
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