Endocannabinoid Signaling Collapse Mediates Stress-Induced Amygdalo-Cortical Strengthening

Marcus, David J.; Bedse, Gaurav; Gaulden, Andrew D.; Ryan, James D.; Kondev, Veronika; Winters, Nathan D.; Rosas-Vidal, Luis E.; Altemus, Megan; Mackie, Ken; Lee, Francis S.; Delpire, Eric; Patel, Sachin

doi:10.1016/j.neuron.2019.12.024

Cited by 104Cannabis and Cannabinoid ResearchNeuroscience and Neuropharmacology ResearchStress Responses and Cortisol

Endocannabinoid Signaling Collapse Mediates Stress-Induced Amygdalo-Cortical Strengthening

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Marcus, David J., Bedse, Gaurav, Gaulden, Andrew D., Ryan, James D., Kondev, Veronika, Winters, Nathan D., Rosas-Vidal, Luis E., Altemus, Megan +4 more·2020·Neuron

DOI 10.1016/j.neuron.2019.12.024PMC PMC7992313

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Abstract

Functional coupling between the amygdala and the dorsomedial prefrontal cortex (dmPFC) has been implicated in the generation of negative affective states; however, the mechanisms by which stress increases amygdala-dmPFC synaptic strength and generates anxiety-like behaviors are not well understood. Here, we show that the mouse basolateral amygdala (BLA)-prelimbic prefrontal cortex (plPFC) circuit is engaged by stress and activation of this pathway in anxiogenic. Furthermore, we demonstrate that acute stress exposure leads to a lasting increase in synaptic strength within a reciprocal BLA-plPFC-BLA subcircuit. Importantly, we identify 2-arachidonoylglycerol (2-AG)-mediated endocannabinoid signaling as a key mechanism limiting glutamate release at BLA-plPFC synapses and the functional collapse of multimodal 2-AG signaling as a molecular mechanism leading to persistent circuit-specific synaptic strengthening and anxiety-like behaviors after stress exposure. These data suggest that circuit-specific impairment in 2-AG signaling could facilitate functional coupling between the BLA and plPFC and the translation of environmental stress to affective pathology.

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Synaptic connections between PL neurons and BLA inputs strengthen in response to stress, in part through endocannabinoid-mediated mechanisms.
“Synaptic connections between PL neurons and BLA inputs also strengthen in response to stress, in part through endocannabinoid-mediated mechanisms [52].”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [52]

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Robinson OJ, Krimsky M, Lieberman L, Allen P, Vytal K, and Grillon C (2014). Towards a mechanistic understanding of pathological anxiety: the dorsal medial prefrontal-amygdala ‘aversive amplification’ circuit in unmedicated generalized and social anxiety disorders. Lancet Psychiatry 1, 294– 302. 25722962 PMC4337019

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Authors: Marcus, D. J., Bedse, G., Gaulden, A. D., Ryan, J. D., Kondev, V., Winters, N. D., Rosas-Vidal, L. E., Altemus, M., Mackie, K., Lee, F. S., Delpire, E., & Patel, S.
Affiliations: Vanderbilt University (US)
Vanderbilt University Medical Center (US)
Weill Cornell Medicine (US)
Indiana University Bloomington (US)
Corresponding author: Patel, Sachin
ORCID: Marcus, David J.
Bedse, Gaurav
Kondev, Veronika
Winters, Nathan D.
Rosas-Vidal, Luis E.
Altemus, Megan
Mackie, Ken
Lee, Francis S.
Delpire, Eric
Patel, Sachin
Venue: Neuron
Publisher: Elsevier BV
Published: 2020-03
Volume: 105
Issue: 6
Pages: 1062-1076.e6
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2019.12.024
PMC: PMC7992313
OpenAlex: W2946990124
Cited by: 104
References: 95
Citations by year: 2026: 12 · 2025: 17 · 2024: 19 · 2023: 12 · 2022: 13 · 2021: 17 · 2020: 14
FWCI: 8.39
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, 382 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)
SSRN Electronic Journal (acceptedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (DA043982, MH107435, MH114363, NS052819)
Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (AA9013514)
National Alliance for Research on Schizophrenia and Depression
Topics: Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: endocannabinoid signaling, 2-arachidonoylglycerol, acute stress, anxiety-like behavior, basolateral amygdala, prelimbic cortex, synaptic plasticity, glutamate release, stress-induced anxiety
MeSH terms: Animals, Anxiety, Arachidonic Acids, Glycerides, Male, Neural Pathways, Synaptic Transmission, Restraint, Physical, Stress, Psychological, Prefrontal Cortex, Glutamic Acid, Mice, Endocannabinoids, Basolateral Nuclear Complex

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Endocannabinoid Signaling Collapse Mediates Stress-Induced Amygdalo-Cortical Strengthening

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