Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray
Open accessAbstract
A form of aversively motivated learning called fear conditioning occurs when a neutral conditioned stimulus is paired with an aversive unconditioned stimulus (UCS). UCS-evoked depolarization of amygdala neurons may instruct Hebbian plasticity that stores memories of the conditioned stimulus-unconditioned stimulus association, but the origin of UCS inputs to the amygdala is unknown. Theory and evidence suggest that instructive UCS inputs to the amygdala will be inhibited when the UCS is expected, but this has not been found during fear conditioning. We investigated neural pathways that relay information about the UCS to the amygdala by recording neurons in the amygdala and periaqueductal gray (PAG) of rats during fear conditioning. UCS-evoked responses in both amygdala and PAG were inhibited by expectation. Pharmacological inactivation of the PAG attenuated UCS-evoked responses in the amygdala and impaired acquisition of fear conditioning, indicating that PAG may be an important part of the pathway that relays instructive signals to the amygdala.
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Periaqueductal gray neurons respond more strongly to unexpected than expected electric shocks, consistent with the fMRI findings.
“PAG neurons respond more strongly to unexpected vs. expected electric shocks18, consistent with our fMRI findings here.”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [18]
The periaqueductal gray sends monosynaptic reciprocal projections to ventromedial prefrontal cortex and to anterior mid-cingulate cortex, orbitofrontal cortex, and other areas involved in action value and defensive behavior.
“It also sends monosynaptic, reciprocal projections to the vmPFC—which is essential for value updating in the RL framework and likely for behavioral choice as well31—and to aMCC32, OFC and other areas involved in determining action value and coordinating defensive behavior18,33.”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [18]
The anterior mid-cingulate cortex is critical for pain avoidance and is heavily connected to motor and premotor centers.
“The aMCC in particular is critical for pain avoidance18 and is heavily connected to motor and premotor centers (aMCC).”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [18]
Animal models of fear conditioning suggest that regions encoding avoidance value receive prediction error signals generated in the PAG.
“Based on existent animal models of fear conditioning1,18, we posited that these regions receive the PE signals generated in PAG.”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [18]
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- Authors
- Johansen, J. P., Tarpley, J. W., LeDoux, J. E., & Blair, H. T.
- Affiliations
- University of California, Los Angeles (US)
- Nathan Kline Institute for Psychiatric Research (US)
- Corresponding author
- Tarpley, Jason W
- Blair, Hugh T
- Venue
- Nature Neuroscience
- Published
- 2010-07-04
- Volume
- 13
- Issue
- 8
- Pages
- 979-986
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC2910797
- OpenAlex
- W2112569537
- Cited by
- 312
- References
- 65
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 20 · 2023: 26 · 2022: 26 · 2021: 25 · 2020: 21 · 2019: 19 · 2018: 24 · 2017: 22 · 2016: 24 · 2015: 22 · 2014: 17 · 2013: 12 · 2012: 11
- FWCI
- 7.56
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health
- National Institute of Mental Health (R01MH073700)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- fear conditioning, periaqueductal gray, amygdala, expectations, Hebbian plasticity, fear memory, neural pathways, pharmacological inactivation
- MeSH terms
- Amygdala, Animals, Conditioning, Classical, Electrodes, Implanted, Electrophysiology, Evoked Potentials, Fear, Learning, Male, Neural Pathways, Neurons, Periaqueductal Gray, Rats, Long-Evans, Rats
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