Corticoamygdala Transfer of Socially Derived Information Gates Observational Learning
Open accessAbstract
Observational learning is a powerful survival tool allowing individuals to learn about threat-predictive stimuli without directly experiencing the pairing of the predictive cue and punishment. This ability has been linked to the anterior cingulate cortex (ACC) and the basolateral amygdala (BLA). To investigate how information is encoded and transmitted through this circuit, we performed electrophysiological recordings in mice observing a demonstrator mouse undergo associative fear conditioning and found that BLA-projecting ACC (ACC→BLA) neurons preferentially encode socially derived aversive cue information. Inhibition of ACC→BLA alters real-time amygdala representation of the aversive cue during observational conditioning. Selective inhibition of the ACC→BLA projection impaired acquisition, but not expression, of observational fear conditioning. We show that information derived from observation about the aversive value of the cue is transmitted from the ACC to the BLA and that this routing of information is critically instructive for observational fear conditioning. VIDEO ABSTRACT.
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Projections from the anterior cingulate cortex and insula to the basolateral amygdala have been implicated in social transfer of fear.
“Projections from the ACC and insula to the BLA have been implicated in this form of emotional contagion.”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [102]
Inhibition of anterior cingulate cortex-to-nucleus accumbens core projections did not influence the social transfer of fear, which was reduced by inhibition of anterior cingulate cortex-to-basolateral amygdala projections.
“Surprisingly this same manipulation did not influence the social transfer of fear, which was reduced by inhibition of ACC-to-BLA projections, as previously demonstrated [102].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [102]
Inhibition of anterior cingulate cortex projections to the basolateral amygdala prevents the acquisition of fear, as assessed by freezing, in observer mice.
“Specifically, there is an increase in ACC activity in voles exposed to a stressed partner [93] and inhibition of ACC projections to the BLA prevents the acquisition of fear, as assessed by freezing, in observer mice [98,102,103].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [102]
Prior investigations in rodents and primates have provided evidence for neurons that encode information about other individuals, demonstrating changes in activity when animals observe another's appetitive or aversive experiences.
“Prior investigations in rodents and primates, for example, have provided evidence for the presence of neurons that encode information about other individuals, demonstrating changes in activity when the animals observe another’s appetitive or aversive experiences 1–11.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [8]
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Valence coding in amygdala circuits
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A neural manifold view of the brain
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Dopamine tunes prefrontal outputs to orchestrate aversive processing
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Neural mechanisms necessary for empathy-related phenomena across species
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Expressions of emotions across species
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Amygdala connectivity and implications for social cognition and disorders
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Frontal neurons driving competitive behaviour and ecology of social groups
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Social neuroscience of disgust
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Anterior Cingulate Cortex Signals Attention in a Social Paradigm that Manipulates Reward and Shock
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Biological mechanisms for observational learning
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The role of pain modulation pathway and related brain regions in pain
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Neural Circuits for Social Interactions: From Microcircuits to Input-Output Circuits
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Neural correlates and determinants of approach–avoidance conflict in the prelimbic prefrontal cortex
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Similar levels of emotional contagion in male and female rats
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Affective empathy and prosocial behavior in rodents
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A corticoamygdalar pathway controls reward devaluation and depression using dynamic inhibition code
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How Early Life Adversity Influences Defensive Circuitry
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Brain-wide electrical dynamics encode individual appetitive social behavior
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Valence processing in the PFC: Reconciling circuit-level and systems-level views
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Deconstructing the neural circuit underlying social hierarchy in mice
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Dopamine and Serotonin Are Both Required for Mate-Copying in Drosophila melanogaster
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Shared yet dissociable neural codes across eye gaze, valence and expectation
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A prefrontal-thalamic circuit encodes social information for social recognition
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A distinct cortical code for socially learned threat
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The human social cognitive network contains multiple regions within the amygdala
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Neuronal Circuits for Social Decision-Making and Their Clinical Implications
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Physiological synchrony predicts observational threat learning in humans
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Top2a promotes the development of social behavior via PRC2 and H3K27me3
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Dorsomedial prefrontal hypoexcitability underlies lost empathy in frontotemporal dementia
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Prefrontal-amygdala plasticity enabled by observational fear
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A dyad shows mutual changes during social buffering of conditioned fear responses in male rats
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Neural mechanisms of comforting: Prosocial touch and stress buffering
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Ability to share emotions of others as a foundation of social learning
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Observational learning promotes hippocampal remote awake replay toward future reward locations
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- Authors
- Allsop, S. A., Wichmann, R., Mills, F., Burgos-Robles, A., Chang, C.-J., Felix-Ortiz, A. C., Vienne, A., Beyeler, A., Izadmehr, E. M., Glober, G., Cum, M. I., Stergiadou, J., Anandalingam, K. K., Farris, K., Namburi, P., Leppla, C. A., Weddington, J. C., Nieh, E. H., Smith, A. C., Ba, D., Brown, E. N., & Tye, K. M.
- Affiliations
- Massachusetts Institute of Technology (US)
- University of Arizona (US)
- Harvard University (US)
- Corresponding author
- Tye, Kay M.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-05
- Volume
- 173
- Issue
- 6
- Pages
- 1329-1342.e18
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6345560
- OpenAlex
- W2799513798
- Cited by
- 288
- References
- 64
- Citations by year
- 2026: 26 · 2025: 30 · 2024: 42 · 2023: 37 · 2022: 33 · 2021: 43 · 2020: 28 · 2019: 26 · 2018: 23
- FWCI
- 17.72
- 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, 395 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
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- JPB Foundation
- PIIF
- PNDRF
- JFDP
- Whitehall Foundation
- Klingenstein Foundation
- NARSAD Young Investigator Award
- Alfred P. Sloan Foundation
- New York Stem Cell Foundation
- McKnight Foundation
- Whitehead Career Development Chair
- NIMH (R01-MH102441-01)
- NIA (RF1-AG047661-01)
- NIH (DP2-DK-102256-01, DP1-AT009925, 1-R01-AG-050548-01, DP1-OD003646, R01-GM104948)
- Jeffrey and Nancy Halis Fellowship
- Henry E. Singleton Fund
- NLM
- Simons Center for the Social Brain
- Netherlands Organization for Scientific Research
- NARSAD
- Brain & Behavior Research Foundation
- National Research Service (5T32GM007484-38)
- Canadian Institutes of Health
- Swiss National Science Foundation
- NSF Graduate Research Fellowships (T32 GM007484)
- Training Program in the Neurobiology of Learning and Memory
- Singleton
- Leventhal
- Whitaker
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- observational learning, fear conditioning, anterior cingulate cortex, basolateral amygdala, social learning, mice
- MeSH terms
- Amygdala, Animals, Behavior, Animal, Cerebral Cortex, Conditioning, Classical, Fear, Learning, Light, Male, Memory, Neural Pathways, Neurons, Prefrontal Cortex, Mice, Electrophysiological Phenomena, Optogenetics, Basolateral Nuclear Complex
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