Cited by 288Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

Corticoamygdala Transfer of Socially Derived Information Gates Observational Learning

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Allsop, Stephen A., Wichmann, Romy, Mills, Fergil, Burgos-Robles, Anthony, Chang, Chia-Jung, Felix-Ortiz, Ada C., Vienne, Alienor, Beyeler, Anna +14 more·2018·Cell

Abstract

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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Crossref · 10.1016/j.cell.2018.04.004

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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.”

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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.
Venue
Cell
Publisher
Elsevier BV
Published
2018-05
Volume
173
Issue
6
Pages
1329-1342.e18
ISSN
0092-8674 (ISSN-L)
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
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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