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Distribution of CB1 Cannabinoid Receptors in the Amygdala and their Role in the Control of GABAergic Transmission
Open accessAbstract
Cannabinoids are the most popular illicit drugs used for recreational purposes worldwide. However, the neurobiological substrate of their mood-altering capacity has not been elucidated so far. Here we report that CB1 cannabinoid receptors are expressed at high levels in certain amygdala nuclei, especially in the lateral and basal nuclei, but are absent in other nuclei (e.g., in the central nucleus and in the medial nucleus). Expression of the CB1 protein was restricted to a distinct subpopulation of GABAergic interneurons corresponding to large cholecystokinin-positive cells. Detailed electron microscopic investigation revealed that CB1 receptors are located presynaptically on cholecystokinin-positive axon terminals, which establish symmetrical GABAergic synapses with their postsynaptic targets. The physiological consequence of this particular anatomical localization was investigated by whole-cell patch-clamp recordings in principal cells of the lateral and basal nuclei. CB1 receptor agonists WIN 55,212-2 and CP 55,940 reduced the amplitude of GABA(A) receptor-mediated evoked and spontaneous IPSCs, whereas the action potential-independent miniature IPSCs were not significantly affected. In contrast, CB1 receptor agonists were ineffective in changing the amplitude of IPSCs in the rat central nucleus and in the basal nucleus of CB1 knock-out mice. These results suggest that cannabinoids target specific elements in neuronal networks of given amygdala nuclei, where they presynaptically modulate GABAergic synaptic transmission. We propose that these anatomical and physiological features, characteristic of CB1 receptors in several forebrain regions, represent the neuronal substrate for endocannabinoids involved in retrograde synaptic signaling and may explain some of the emotionally relevant behavioral effects of cannabinoid exposure.
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“Following their synthesis, ECBs are retrogradely transported into the extracellular space to bind ECB receptors present on presynaptic terminals [19–21].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [19]
In the citing paper
“Within amygdala subnuclei, FAAH is highly expressed on pyramidal neurons in the BLA, and to a significantly lesser extent in the central nucleus (CeA) [19,20,46,47].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [19]
In the citing paper
“Yet, CB1 receptors are expressed at high levels in the BLA (Herkenham et al, 1990;Katona et al, 2001;Tsou et al, 1997)”
From Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress (2012) · cites this paper as Katona et al, 2001
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“but their expression in the central amygdala is less clear (Katona et al, 2001;Tsou et al, 1997;Cota et al, 2007; but see Kamprath et al, 2011).”
From Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress (2012) · cites this paper as Katona et al, 2001
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“(3) Cannabinoids are in widespread use recreationally as psychoactive drugs and interact with other drugs of abuse, which emphasizes even more the need to understand the eCB system and the neurobiological substrate of their mood-altering capacity (Katona et al., 2001; Valjent et al., 2002), e.”
BackgroundWIN 55,212-2 decreases the spatial spread of neocortical excitation in vitro
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“Nonetheless, CB1 receptor numbers are particularly pronounced in areas of the brain normally associated with memory and cognition including areas of the hippocampus, dorsal striatum, amygdala, and a number of cortical regions including the prefrontal cortex [51-53].”
BackgroundMolaei, M., Sanati, M. H., Zaringhalam, J., & Haghparast, A. (2014) · PubMed Central · Cited by 6
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Nasehi, M., Roghani, F., Ebrahimi-Ghiri, M., & Zarrindast, M. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.03.008 · Cited by 6
“studies have confirmed a dense expression of cannabinoid CB1 receptors not only on the GABAergic interneurons (Katona et al., 2001; Tsou et al., 1999) but also the glutamatergic pyramidal projection neurons in the BLA (Nyilas et al.”
Song, S., Kong, X., Borlongan, C. V., Sava, V., & Sanchez‐Ramos, J. (2020) · Cannabis and Cannabinoid Research · doi:10.1089/can.2019.0090 · Cited by 6
Effect of Fatty Acid Amide Hydrolase Inhibitor URB597 on Orofacial Pain Perception in Rats
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Cannabinoids and the Central Serotonergic System
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Pharmacological Studies of the Molecular Basis of Memory Extinction
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“The possibility of such a role is strengthened by the findings on endocannabinoids mentioned above [76], since the drugs affect GABAergic transmission and are present mostly in GABAergic neurons [66, 68 , 76].”
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Lu, H., Roeder, N. M., Richardson, B., Hamilton, J., Sharma, A., Owada, Y., Kagawa, Y., & Thanos, P. K. (2024) · Neuroscience Letters · doi:10.1016/j.neulet.2024.138040 · Cited by 5
Manna, S. S. S. (2022) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000700 · Cited by 5
“These reports are in support with immunohistochemical studies demonstrating the localization of the CB 1 receptors on GABAergic interneurons in cortical areas (Marsicano et al., 1999, 2002; Katona et al., 2001; Alger, 2002; Freund et al., 2003; Chevaleyre et al., 2006; Hill et al., 2007), and on glutamatergic neurons…”
ResultImaging and Genetic Tools for the Investigation of the Endocannabinoid System in the CNS
Kouchaeknejad, A., van der Walt, G., de Donato, M. H., & Puighermanal, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115829 · Cited by 6
“Katona et al. assessed CB1R expression in the amygdala and elucidated its role in GABAergic synaptic transmission [60].”
BackgroundLightfoot, S. H. M., Baglot, S. L., Hume, C., Grace, L. M., McLaughlin, R. J., & Hill, M. N. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107263 · Cited by 4
Canonical Cannabinoid Receptors
Ehrlich, B., Patel, M., Zheng, X., & Glass, M. (2024) · Current topics in behavioral neurosciences · doi:10.1007/7854_2024_556 · Cited by 5
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“…et al., 2023; Jiang et al., 2009). eCBs are hetero-geneously modifiable neurotransmitters that decrease BLA glutamatergic neuronal activity while increasing GABAergic neuronal activity upon binding to presynaptic cannabinoid type 1 (CB1) receptors (Katona et al., 2001; Yoshida et al., 2011).”
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“We focused on the volume of the hippocampus and amygdala given their high density of cannabinoid receptors (35, 36).”
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Distribution of CB1 cannabinoid receptors in the rat amygdaloid complex
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“48 CB1 receptors may drive volumetric changes detected in cannabis users, as they are targeted by cannabis main psychoactive compound delta-9-tetrahydrocannabinol (THC) 49 and may therefore be vulnerable to repeated cannabinoid exposure.”
InfluentialCannabinoid Receptors and Their Signaling Mechanisms
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“85 These areas contain portions of the critical pathways of memory processing, and use of exogenouscannabinoidscandisruptthesepathways.”
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“CB1R in these regions facilitates modulation of voluntary movement, the descending pain pathway, serotonergic neurotransmission, and reticular integration (Caminero and Cascella, 2024).”
InfluentialCannabis, cannabinoids, and receptor responses
Yang, Y., Derwish, R., & Kotra, L. P. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-89862-1.00025-8 · Cited by 3
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“Katona et al. [32] reported that CB1R is predominantly localized presynaptically on the terminals of a specific subset of GABAergic interneurons that co-express cholecystokinin (CCK).”
Cannabinoid-Opioid Interactions
Miller, M. L., Chadwick, B. J., Morris, C. V., Michaelides, M., & Hurd, Y. L. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_15 · Cited by 3
“with this receptor’s neocortical and hippocampal expression [87–89].”
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“Within the amygdala, CB1 receptors are abundant and presynaptically present only on GABAergic interneurons, which inhibit glutamatergic pyramidal neurons [22].”
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“50,51 Consequently, this may have affected GABAergic 112–115 and glutamatergic pathways also highly expressed in the hippocampus and amygdala, which project to other cortical pathways, 102,116,117 potentially changing their functional connectivity.”
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“1 A ), a neurochemical marker that defines this basket cell type in cortical structures together with CCK content (Bodor et al., 2005; Katona et al., 1999; Katona et al., 2001; Koukouli et al., 2022; Nagy-Pal et al., 2023; Varga et al., 2010).”
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“This is in accordance with the fact that both glucocorticoid receptors and CB1 receptors are located within this brain circuit [37–40].”
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“Since Katona and colleagues ’ pivotal revelation of the CB1Rs distribution in the amygdala and its role in controlling gabaergic transmission in 2001 (Katona et al., 2001), numerous studies have explored the concentration of CBRs in the brain.”
BackgroundSun, Y., Sivasubramanian, M., Milenkovic, M., Gumbert, A. B., Bergman, J., Ge, P., Heiman, M., Raddo, M.-E. D., Withey, S. L., Madras, B. K., et al. (2025) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2025.100496 · Cited by 1
“Cannabinoids affect multiple brain regions that express relatively high levels of endocannabinoid system components, including the amygdala (14).”
Tokutake, T., Yokose, J., Yano, Y., Shigetsura, Y., Muramatsu, S., & Nitta, A. (2025) · Behavioral and Brain Functions · doi:10.1186/s12993-025-00306-w · Cited by 1
“They are abundantly expressed in cholecystokinin (CCK)-positive interneurons in the brain [37, 39, 40].”
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“CB1Rs are predominantly located on presynaptic terminals throughout the mesolimbic system, including on glutamatergic afferents to the nucleus accumbens and on GABAergic interneurons in the basolateral amygdala (Covey and Yocky 2021; Katona et al. 2001; Peters et al. 2021; Winters et al. 2012).”
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“Central CB1 receptors are expressed at high levels in www.intechopen.com Anxiety Disorders 166 the lateral and basal nuclei of the amygdala (Katona et al., 2001), and extinction of aversive memories depends on cannabinoid receptors and signalling within the BLA (Marsicano et al., 2002; Kamprath et…”
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“Within the BLA, CB1 receptors are in particular abundantly expressed in GABAergic interneurons (Katona et al. 2001) and activation of CB1 receptors has consistently been shown to suppress the release of GABA (Katona et al.”
BackgroundCannabis chez les enfants et les adolescents : impacts et conséquences
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Metadata
- Authors
- Katona, I., Rancz, E. A., Acsády, L., Ledent, C., Mackie, K., Hájos, N., & Freund, T. F.
- Affiliations
- HUN-REN Institute of Experimental Medicine (HU)
- Université Libre de Bruxelles (BE)
- University of Washington (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-12-01
- Volume
- 21
- Issue
- 23
- Pages
- 9506-9518
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6763903
- OpenAlex
- W2153392906
- Cited by
- 668
- References
- 59
- Citations by year
- 2026: 10 · 2025: 22 · 2024: 18 · 2023: 20 · 2022: 31 · 2021: 29 · 2020: 33 · 2019: 18 · 2018: 20 · 2017: 36 · 2016: 37 · 2015: 34 · 2014: 27 · 2013: 29 · 2012: 26
- FWCI
- 13.43
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Hungarian Scientific Research Fund (T032251)
- National Institutes of Health (5k01da000285-04)
- National Institute on Drug Abuse (DA 00285, DA11322, R01DA011322)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 41301, P30DK041301)
- National Institute of Neurological Disorders and Stroke (NS30549)
- Topics
- Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- CB1 receptor, amygdala, GABAergic neurotransmission, cholecystokinin interneurons, presynaptic modulation, endocannabinoids, lateral amygdala, basal amygdala, cannabinoid receptor agonists, CB1 knockout mice, emotional behavior
- MeSH terms
- Amygdala, Analgesics, Animals, Cannabinoids, Cholecystokinin, Cyclohexanols, gamma-Aminobutyric Acid, Interneurons, Male, Membrane Potentials, Morpholines, Naphthalenes, Nerve Net, Neural Inhibition, Synaptic Transmission, Organ Specificity, Receptors, Drug, Receptors, GABA-A, Rats, Wistar, Presynaptic Terminals, Mice, Knockout, Patch-Clamp Techniques, Receptors, Cannabinoid, Benzoxazines, Mice, Rats, Cannabinoid Receptor Modulators
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