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Hippocampus-driven feed-forward inhibition of the prefrontal cortex mediates relapse of extinguished fear

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Marek, Roger, Jin, Jingji, Goode, Travis D., Giustino, Thomas F., Wang, Qian, Acca, Gillian M., Holehonnur, Roopashri, Ploski, Jonathan E., Fitzgerald, Paul J., Lynagh, Timothy, Lynch, Joseph W., Maren, Stephen, Sah, Pankaj·2018·Nature Neuroscience

DOI 10.1038/s41593-018-0073-9PMC PMC5957529

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Abstract

The medial prefrontal cortex (mPFC) has been implicated in the extinction of emotional memories, including conditioned fear. We found that ventral hippocampal (vHPC) projections to the infralimbic (IL) cortex recruited parvalbumin-expressing interneurons to counter the expression of extinguished fear and promote fear relapse. Whole-cell recordings ex vivo revealed that optogenetic activation of vHPC input to amygdala-projecting pyramidal neurons in the IL was dominated by feed-forward inhibition. Selectively silencing parvalbumin-expressing, but not somatostatin-expressing, interneurons in the IL eliminated vHPC-mediated inhibition. In behaving rats, pharmacogenetic activation of vHPC→IL projections impaired extinction recall, whereas silencing IL projectors diminished fear renewal. Intra-IL infusion of GABA receptor agonists or antagonists, respectively, reproduced these effects. Together, our findings describe a previously unknown circuit mechanism for the contextual control of fear, and indicate that vHPC-mediated inhibition of IL is an essential neural substrate for fear relapse.

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Authors: Marek, R., Jin, J., Goode, T. D., Giustino, T. F., Wang, Q., Acca, G. M., Holehonnur, R., Ploski, J. E., Fitzgerald, P. J., Lynagh, T., Lynch, J. W., Maren, S., & Sah, P.
Affiliations: The University of Queensland (AU)
Texas A&M University (US)
The University of Texas at Dallas (US)
University of Copenhagen (DK)
Corresponding author: Maren, Stephen
Sah, Pankaj
ORCID: Marek, Roger
Jin, Jingji
Goode, Travis D.
Giustino, Thomas F.
Wang, Qian
Ploski, Jonathan E.
Fitzgerald, Paul J.
Lynagh, Timothy
Lynch, Joseph W.
Maren, Stephen
Sah, Pankaj
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2018-02-05
Volume: 21
Issue: 3
Pages: 384-392
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/s41593-018-0073-9
PMC: PMC5957529
OpenAlex: W2797856206
Cited by: 226
References: 59
Citations by year: 2026: 17 · 2025: 21 · 2024: 20 · 2023: 22 · 2022: 24 · 2021: 34 · 2020: 34 · 2019: 30 · 2018: 24
FWCI: 18.17
Type: journal article
Language: en
Update notices: correction (2018-07-09)
Open access: green
www.ncbi.nlm.nih.gov
Licence: other-oa
www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, other-oa)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (F31MH107113, F31MH112208, R01MH065961)
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 extinction, fear relapse, ventral hippocampus, infralimbic cortex, medial prefrontal cortex, feedforward inhibition, parvalbumin interneurons, somatostatin interneurons, extinction recall, fear renewal, GABA receptors, optogenetics, pharmacogenetics
MeSH terms: Amygdala, Animals, Extinction, Psychological, Fear, Hippocampus, Interneurons, Male, Parvalbumins, Somatostatin, Rats, Wistar, Prefrontal Cortex, Receptors, GABA, Patch-Clamp Techniques, Rats

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Hippocampus-driven feed-forward inhibition of the prefrontal cortex mediates relapse of extinguished fear

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