Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic–pituitary–adrenal axis
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Endocannabinoids inhibit hypothalamic-pituitary-adrenal (HPA) axis activity; however, the neural substrates and pathways subserving this effect are not well characterized. The amygdala is a forebrain structure that provides excitatory drive to the HPA axis under conditions of stress. The aim of this study was to determine the contribution of endocannabinoid signaling within distinct amygdalar nuclei to activation of the HPA axis in response to psychological stress. Exposure of rats to 30-min restraint stress increased the hydrolytic activity of fatty acid amide hydrolase (FAAH) and concurrently decreased content of the endocannabinoid/CB(1) receptor ligand N-arachidonylethanolamine (anandamide; AEA) throughout the amygdala. In stressed rats, AEA content in the amygdala was inversely correlated with serum corticosterone concentrations. Pharmacological inhibition of FAAH activity within the basolateral amygdala complex (BLA) attenuated stress-induced corticosterone secretion; this effect was blocked by co-administration of the CB(1) receptor antagonist AM251, suggesting that stress-induced decreases in CB(1) receptor activation by AEA contribute to activation of the neuroendocrine stress response. Local administration into the BLA of a CB(1) receptor agonist significantly reduced stress-induced corticosterone secretion, whereas administration of a CB(1) receptor antagonist increased corticosterone secretion. Taken together, these findings suggest that the degree to which stressful stimuli reduce amygdalar AEA/CB(1) receptor signaling contributes to the magnitude of the HPA response.
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Most effects of lipid signaling molecules on stress and memory are central.
“Other limitations of our study result from the fact that we measured peripheral plasma concentrations of ECs/NAEs whereas most effects of lipid signaling molecules on stress and memory are central [13]–[15], [44].”
From Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder (2013) · cites this paper as [44]
Increasing AEA by inhibiting FAAH with URB597 reduces the HPA axis and anxiety-like response to stress.
“Second, increasing AEA by inhibiting FAAH (with URB597) reduces the HPA axis and anxiety-like response to stress [58,66].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [58]
CB1R antagonism increases BLA excitability, activates the HPA axis, and increases anxiety-like behavior.
“First, presumably by removing AEA-mediated tonic inhibitory activity, CB1R antagonism increases BLA excitability [61–63], activates the hypothalamic–pituitary–adrenal (HPA) axis and increases anxiety-like behavior [58,64,65].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [58]
Stress produces divergent effects on AEA and 2-AG levels in the BLA, with an elevation in 2-AG levels and a rapid induction of FAAH activity and resultant decline in the AEA pool following exposure to various types of stress.
“Interestingly, stress appears to produce divergent effects on AEA and 2-AG levels in the BLA – with an elevation in 2-AG levels [57], but a rapid induction of FAAH activity and a resultant decline in the pool of AEA [58–60] were reported following exposure to various types of stress.”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [58]
The anti-stress effects of FAAH inhibition are localized specifically within the BLA: only infusion of URB597 into the BLA, and not CeA or medial amygdala, is effective.
“These actions of FAAH inhibition have been localized to actions specifically within the BLA by the finding that only infusion of URB597 into the BLA, and not CeA or medial amygdala, is effective in producing these anti-stress effects [58].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [58]
AEA content in the BLA is reduced at the termination of restraint stress and is negatively correlated with the magnitude of the CORT response to stress.
“Hill et al (2009) have recently shown that the content of AEA in the BLA is reduced at the termination of restraint stress (also see Patel et al, 2005a andRademacher et al, 2008) and that AEA content is negatively correlated with the magnitude of the CORT response to stress.”
From Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress (2012) · cites this paper as Hill et al, 2009
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- Authors
- Hill, M. N., McLaughlin, R. J., Morrish, A. C., Viau, V., Floresco, S. B., Hillard, C. J., & Gorzalka, B. B.
- Affiliations
- University of British Columbia (CA)
- Medical College of Wisconsin (US)
- Corresponding author
- Hill, Matthew N
- Venue
- Neuropsychopharmacology
- Published
- 2009-08-26
- Volume
- 34
- Issue
- 13
- Pages
- 2733-2745
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC3197779
- OpenAlex
- W2074290211
- Cited by
- 304
- References
- 68
- Citations by year
- 2026: 9 · 2025: 19 · 2024: 12 · 2023: 17 · 2022: 12 · 2021: 25 · 2020: 20 · 2019: 19 · 2018: 20 · 2017: 19 · 2016: 24 · 2015: 29 · 2014: 11 · 2013: 17 · 2012: 17
- FWCI
- 12.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Medical College of Wisconsin
- Michael Smith Health Research BC
- National Institutes of Health
- Canadian Institutes of Health Research
- Natural Sciences and Engineering Research Council of Canada
- National Institute on Drug Abuse (R21DA022439)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- endocannabinoids, amygdala, hypothalamic-pituitary-adrenal axis, psychological stress, restraint stress, fatty acid amide hydrolase, anandamide, CB1 receptor, corticosterone, basolateral amygdala, neuroendocrine stress response, CB1 receptor agonists
- MeSH terms
- Fatty Acid Amide Hydrolases, Amidohydrolases, Amygdala, Animals, Arachidonic Acids, Benzamides, Carbamates, Corticosterone, Drug Interactions, Hypothalamo-Hypophyseal System, Male, Microinjections, Piperidines, Pituitary-Adrenal System, Pyrazoles, Restraint, Physical, Stress, Psychological, Dronabinol, Signal Transduction, Rats, Sprague-Dawley, Receptor, Cannabinoid, CB1, Rats, Polyunsaturated Alkamides, Cannabinoid Receptor Modulators, Endocannabinoids
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