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 synthesis, ECBs are retrogradely transported into the extracellular space to bind ECB receptors present on presynaptic terminals.
“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]
Within amygdala subnuclei, FAAH is highly expressed on pyramidal neurons in the BLA, and to a significantly lesser extent in the central nucleus (CeA).
“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]
CB1 receptors are expressed at high levels in the BLA.
“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
CB1 receptor expression in the central amygdala is less clear.
“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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“…emotion and motivation [i.e., the prefrontal cortex, nucleus accumbens, amygdala, and hypothalamus (Tsou et al., 1998a,b; Marsicano and Lutz, 1999; Katona et al., 2001; McDonald and Mascagni, 2001; Gulyas et al., 2004)] is also consistent with a role for this system in the regulation of emotional…”
BackgroundResultCannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling
Puighermanal, E., Marsicano, G., Busquets-García, A., Lutz, B., Maldonado, R. J., & Ozaita, A. (2009) · Nature Neuroscience · doi:10.1038/nn.2369 · Cited by 381 · see citing works
Enhancing Cannabinoid Neurotransmission Augments the Extinction of Conditioned Fear
Chhatwal, J. P., Davis, M., Maguschak, K. A., & Ressler, K. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300655 · Cited by 376 · see citing works
“…by the dense expression of the CB1 receptor in regions known to be important for anxiety and emotional learning, including the amygdala, hippocampus, and throughout the mesolimbic dopamine reward system (Katona et al, 1999, 2000, 2001; Freund et al, 2003; van der Stelt and Di Marzo, 2003).”
BackgroundUchigashima, M., Narushima, M., Fukaya, M., Katona, I., Kano, M., & Watanabe, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0448-07.2007 · Cited by 375 · see citing works
“Intense perikaryal labeling was reported for CCK-positive interneurons in the hippocampus, cerebral cortex, and amygdala (Katona et al., 1999, 2001; Hajos et al., 2000; Fukudome et al., 2004; Bodor et al., 2005) but has never been seen in the striatum (Julian et al., 2003; Matyas et al., 2006) (Fig.”
BackgroundGABAA receptor diversity and pharmacology
Möhler, H. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0284-3 · Cited by 359 · see citing works
“The terminals of CCK-positive GABAergic basket cells in hippocampus and amygdala contain CB1-cannabinoid receptors (Katona et al. 1999, 2001).”
BackgroundEgertová, M., Cravatt, B. F., & Elphick, M. R. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00145-3 · Cited by 347 · see citing works
“Accordingly , several recent studies indicate that endocannabinoids also act as retrograde synaptic signaling molecules in these regions of the forebrain (Katona et al., 2001; Trettel and Levine, 2002).”
BackgroundHill, M. N., & Tasker, J. G. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.12.030 · Cited by 341 · see citing works
Bodor, Á. L., Katona, I., Nyíri, G., Mackie, K., Ledent, C., Hájos, N., & Freund, T. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0442-05.2005 · Cited by 325 · see citing works
“Similarly, large CCK-positive cells were found to express CB 1 receptors in both the basolateral amygdala (Katona et al., 2001; McDonald and Mascagni, 2001) and hippocampus (Katona et al., 1999).”
BackgroundLong-term potentiation in the amygdala: A cellular mechanism of fear learning and memory
Sigurdsson, T., Doyère, V., Cain, C. K., & LeDoux, J. E. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.022 · Cited by 325 · see citing works
“, 2005), cannabinoids (Katona et al., 2001; McDonald and Mascagni, 2001; Marsicano et al., 2002) and dopamine (Brinley-Reed and McDonald, 1999; Bissiere et al.”
BackgroundYoshida, T., Fukaya, M., Uchigashima, M., Miura, E., Kamiya, H., Kano, M., & Watanabe, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0054-06.2006 · Cited by 327 · see citing works
“…mice have provided evidence that CB1 is the major presynaptic cannabinoid receptor at inhibitory and excitatory synapses in various brain regions (Katona et al., 1999, 2001; Farquhar-Smith et al., 2000; Hajos et al., 2000, 2001; Wilson and Received Jan. 6, 2006; revised March 18, 2006; accepted…”
BackgroundFritschy, J., & Brünig, I. (2003) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(03)00037-8 · Cited by 322 · see citing works
Hill, M. N., McLaughlin, R. J., Morrish, A. C., Viau, V., Floresco, S. B., Hillard, C. J., & Gorzalka, B. B. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.114 · Cited by 304 · see citing works
Ständer, S., Schmelz, M., Metze, D., Luger, T. A., & Rukwied, R. (2005) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2005.01.007 · Cited by 300 · see citing works
“Numerous studies described the expression of cannabinoid 1 receptors in animal and human brain tissue [2,35—39].”
BackgroundPatel, S., Roelke, C. T., Rademacher, D. J., & Hillard, C. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03916.x · Cited by 297 · see citing works
“…European Journal of Neuroscience, 21, 1057–1069 within subregions of the amygdala (Patel et al., 2004a) and the known cellular and functional effects of eCB signalling previously observed in this region (Alonso et al., 1999; Katona et al., 2001; Marsicano et al., 2002; Azad et al., 2003).”
BackgroundCampolongo, P., Roozendaal, B., Trezza, V., Hauer, D., Schelling, G., McGaugh, J. L., & Cuomo, V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900835106 · Cited by 294 · see citing works
“CB1 receptors are expressed at high levels in the rat amygdala, particularly the BLA (4, 13, 28).”
BackgroundManzanares, J., Julian, M., & Carrascosa, A. (2006) · Current Neuropharmacology · doi:10.2174/157015906778019527 · Cited by 287 · see citing works
“Their distribution has been mapped by autoradiographic studies, immunohistochemical techniques, in situ histochemistry, and electrophysiological studies [53, 78, 140].”
Eggan, S. M., & Lewis, D. A. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj136 · Cited by 261 · see citing works
Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling
Azad, S. C., Monory, K., Marsicano, G., Cravatt, B. F., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2134-04.2004 · Cited by 263 · see citing works
Amygdala Inhibitory Circuits Regulate Associative Fear Conditioning
Krabbe, S., Gründemann, J., & Lüthi, A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.10.006 · Cited by 255 · see citing works
“Abbreviations: PN: principal neuron, CS: conditioned stimulus, US: unconditioned stimulus, IL: infralimbic, PL: prelimbic, CB1R: cannabinoid receptor type 1, DGLα: diacylglycerol lipase α, DSI: depolarization-induced suppression of inhibition.”
BackgroundInfluentialEffects of Cannabinoids on Neurotransmission
Szabó, B., & Schlicker, E. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_11 · Cited by 256 · see citing works
“In the other method, the release of endogenous or radiolabelled neurotransmitters from presynaptic axon terminals is determined chemically.”
BackgroundCannabinoid Modulation of Amygdala Reactivity to Social Signals of Threat in Humans
Phan, K. L., Angstadt, M., Golden, J., Onyewuenyi, I., Popovska, A., & de Wit, H. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5603-07.2008 · Cited by 251 · see citing works
“CB1 receptors are densely localized to a distinct population of GABAergic interneurons in the lateral and basal (BLA), but not central (CeA), nuclei of the amygdala (Katona et al., 2001).”
BackgroundInfluentialEndocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α
Chevaleyre, V., Heifets, B. D., Kaeser, P. S., Südhof, T. C., & Castillo, P. E. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.020 · Cited by 261 · see citing works
“, 2001) but also in the amygdala (Azad et al., 2003;Katona et al., 2001).”
Hariri, A. R., Gorka, A. X., Hyde, L. W., Kimak, M. A., Halder, I., Ducci, F., Ferrell, R. E., Goldman, D. A., & Manuck, S. B. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.047 · Cited by 250 · see citing works
“Such effects of eCB signaling on anxiety-like behaviors are likely mediated through the amygdala, where CB1 receptors are densely expressed (47; 48), and both AEA and 2-AG concentrations are markedly elevated during the presentation of anxiogenic stimuli (49).”
Presynaptic Modulation by Endocannabinoids
Lovinger, D. M. (2007) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-74805-2_14 · Cited by 245 · see citing works
“or other properties of miniature synaptic responses, indicating that the receptor has little effect on mechanisms downstream from VGCCs (Hoffman and Lupica 2001; Katona et al. 2001; Zhu and Lovinger 2005).”
BackgroundKöfalvi, A., Rodrigues, R. J., Ledent, C. A., Mackie, K., Vizi, E. S., Cunha, R. A., & Sperlágh, B. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4232-04.2005 · Cited by 242 · see citing works
“The specificity of CB1 receptor antibody has been confirmed by the laboratory of origin and by the lack of immunostaining in the CB1 receptor knock-out mice (Katona et al., 2001).”
BackgroundHaller, J., Varga, B., Ledent, C., & Freund, T. F. (2004) · Behavioural Pharmacology · doi:10.1097/01.fbp.0000135704.56422.40 · Cited by 241 · see citing works
Neurodevelopment, GABA System Dysfunction, and Schizophrenia
Schmidt, M. J., & Mirnics, K. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.95 · Cited by 239 · see citing works
Hill, M. N., Campolongo, P., Yehuda, R., & Patel, S. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.162 · Cited by 239 · see citing works
“Similarly, studies employing exogenous CB1 receptor agonists have also found that activation of CB1 receptors can suppress both glutamatergic and GABAergic synaptic transmission (Azad et al, 2003; Domenici et al, 2006; Katona et al, 2001).”
BackgroundRademacher, D. J., Meier, S. E., Shi, L., Vanessa Ho, W.-S., Jarrahian, A., & Hillard, C. J. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.06.012 · Cited by 233 · see citing works
The neuropsychopharmacology of cannabis: A review of human imaging studies
Bloomfield, M., Hindocha, C., Green, S. F., Wall, M. B., Lees, R., Petrilli, K., Costello, H., Ogunbiyi, O., Bossong, M. G., & Freeman, T. P. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.10.006 · Cited by 238 · see citing works
“No significant change Ford et al. (2014) fMRI 15 [cannabis users]/15 [MDD]/14 [cannabis users with MDD]/17 [healthy controls] - Music Listening Paradigm (Neutral and Preferred Music) 20.2 (1.3) [cannabis users], 19.9 (1.7) [MDD + cannabis users] 6.8 (0.4) [cannabis users] 6.9 (0.4) [cannabis users + MDD] - 22.0 (6.2)…”
BackgroundInfluentialAmygdala FAAH and anandamide: mediating protection and recovery from stress
Gunduz-Cinar, O., Hill, M. N., McEwen, B. S., & Holmes, A. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.08.008 · Cited by 229 · see citing works
“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].”
BackgroundDomenici, M. R., Azad, S. C., Marsicano, G., Schierloh, A., Wotjak, C. T., Dodt, H.-U., Zieglgänsberger, W., Lutz, B., & Rammes, G. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0372-06.2006 · Cited by 224 · see citing works
Azad, S. C., Eder, M., Marsicano, G., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2003) · Learning & Memory · doi:10.1101/lm.53303 · Cited by 220 · see citing works
“Endocannabinoids are considered to be retrograde messengers released by neurons to modulate release of neurotransmitters (Kreitzer and Regehr 2001; Ohno-Shosaku et al. 2001; Wilson and Nicoll 2001).”
BackgroundCannabinoid Function in Learning, Memory and Plasticity
Riedel, G., & Davies, S. N. (2005) · Springer eBooks · doi:10.1007/3-540-26573-2_15 · Cited by 219 · see citing works
Endocannabinoid mechanisms of pain modulation
Hohmann, A. G., & Suplita, R. L. (2006) · The AAPS Journal · doi:10.1208/aapsj080479 · Cited by 213 · see citing works
Effects of endocannabinoid system modulation on cognitive and emotional behavior
Zanettini, C. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00057 · Cited by 214 · see citing works
Endocannabinoid system in neurodegenerative disorders
Basavarajappa, B. S., Shivakumar, M., Joshi, V., & Subbanna, S. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14098 · Cited by 212 · see citing works
“CB1Rs have been shown to be localized presynaptically on GABAergic interneurons and glutamatergic neurons (Katona et al. 1999, 2001, 2006), and this localization of CB1Rs is consistent with the proposed role of ECs in modulating GABA and glutamate neurotransmission (Ohno-Shosaku et al. 1998, 2000,…”
Interneurons in the basolateral amygdala
Spampanato, J. G., Polepalli, J. S., & Sah, P. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.11.006 · Cited by 205 · see citing works
“…with somata and dendrites as well as presynaptic terminals of CCKþ interneurons where it’s activation produces a short duration reduction of the action potential evoked release of GABA and the subsequent inhibitory post-synaptic current (Katona et al., 2001; McDonald and Mascagni, 2001b).”
BackgroundHájos, N., & Freund, T. F. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00157-0 · Cited by 198 · see citing works
Pistis, M., Perra, S., Pillolla, G., Melis, M., Muntoni, A. L., & Gessa, G. L. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.05.006 · Cited by 194 · see citing works
Hill, M. N., & Gorzalka, B. B. (2005) · Behavioural Pharmacology · doi:10.1097/00008877-200509000-00006 · Cited by 193 · see citing works
“Modest to high CB1 receptor densities exist in structures implicated in depression, including the prefrontal cortex, hypothalamus, amygdala and hippocampus (Herkenham et al., 1991; Marsicano and Lutz, 1999; Tsou et al., 1999; Moldrich and Wenger, 2000; Katona et al., 2001).”
BackgroundEndocannabinoids in Amygdala and Nucleus Accumbens Mediate Social Play Reward in Adolescent Rats
Trezza, V., Damsteegt, R., Manduca, A., Petrosino, S., Van Kerkhof, L. W. M., Pasterkamp, R. J., Zhou, Y., Campolongo, P., Cuomo, V., Di Marzo, V., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0114-12.2012 · Cited by 190 · see citing works
“CB1 cannabinoid receptors are abundant in brain areas involved in emotion and motivation, such as the nucleus accumbens (NAc) and amygdala (Tsou et al., 1998; Katona et al., 2001).”
Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia
Mátyás, F., Yanovsky, Y., Mackie, K., Kelsch, W., Misgeld, U., & Freund, T. F. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.09.005 · Cited by 191 · see citing works
“CB1 is highly expressed by GABAergic neurons in many brain regions, especially in the hippocampus, neocortex, cerebellum, amygdala, as well as in several nuclei of the basal ganglia (Tsou et al., 1998; Katona et al., 1999, 2001; Egertova and Elphick, 2000; Egertova et al., 2003; Freund et al., 2003; Julian et al., 200…”
BackgroundResultMechanisms of memory under stress
Schwabe, L., Hermans, E. J., Joëls, M., & Roozendaal, B. (2022) · Neuron · doi:10.1016/j.neuron.2022.02.020 · Cited by 188 · see citing works
Functionally selective cannabinoid receptor signalling: Therapeutic implications and opportunities
Bosier, B., Muccioli, G. G., Hermans, E., & Lambert, D. M. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.02.013 · Cited by 188 · see citing works
A fluorescent sensor for spatiotemporally resolved imaging of endocannabinoid dynamics in vivo
Dong, A., He, K., Dudok, B., Farrell, J. S., Guan, W., Liput, D. J., Puhl, H. L., Cai, R., Wang, H., Duan, J., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-01074-4 · Cited by 179 · see citing works
Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses
Trouche, S., Sasaki, J. M., Tu, T., & Reijmers, L. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.047 · Cited by 166 · see citing works
“Since CB1R inhibit the release of g-aminobutyric acid (GABA) (Katona et al., 2001), these results suggest that the extinction-induced upregulation of perisomatic CB1R facilitated the persistence of a small subset of active BA fear neurons in the extinction group (Figure 1J).”
InfluentialCellular and molecular connections between sleep and synaptic plasticity
Benington, J. H., & Frank, M. G. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00018-2 · Cited by 244 · see citing works
“CB1 endocannabinoid receptors have been identified in presynaptic terminals (Katona et al., 1999, 2001), enabling endocannabinoids to function as retrograde messengers (Ohno-Shosaku et al., 2001).”
BackgroundEndocannabinoid influence in drug reinforcement, dependence and addiction-related behaviors
Serrano, A., & Parsons, L. H. (2011) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2011.06.005 · Cited by 180 · see citing works
“Moreover, plastic events in regions such as the NAc, PFC and other limbic structures likely participate in the formation of conditioned associations between drug reward and a variety of internal and external cues associated with drug intake.”
BackgroundInfluentialThe endocannabinoid system as a target for the treatment of neurodegenerative disease
Scotter, E. L., Abood, M. E., & Glass, M. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00735.x · Cited by 181 · see citing works
“At the subcellular level, CB1 has been localized to pre-synaptic terminals, and is found at significantly higher levels on GABAergic than glutamatergic neurons in various brain regions (Katona et al., 1999; Katona et al., 2001; Puighermanal et al., 2009).”
CB1 receptor stimulation in specific brain areas differently modulate anxiety-related behaviour
Rubino, T., Guidali, C., Viganò, D., Realini, N., Valenti, M., Massi, P., & Parolaro, D. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.06.024 · Cited by 179 · see citing works
The basolateral amygdala γ‐aminobutyric acidergic system in health and disease
Prager, E. M., Bergstrom, H. C., Wynn, G. H., & Braga, M. F. M. (2015) · Journal of Neuroscience Research · doi:10.1002/jnr.23690 · Cited by 178 · see citing works
“…widely distributed in the brain but are present in relatively high concentrations in the BLA and, in particular, are present on the presynaptic terminal of CCK interneurons (Katona et al., 2001; McDonald and Mascagni, 2001b), which densely innervate principal neurons (McDonald and Pearson, 1989).”
InfluentialDistribution of the Endocannabinoid System in the Central Nervous System
Hu, S. S., & Mackie, K. (2015) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-20825-1_3 · Cited by 177 · see citing works
“Although the distribution of CB1 immunoreactivity across monkey neocortical regions is broadly similar to that observed in the rat using immunocytochemical (Egertova and Elphick 2000; Hajos et al. 2000; Katona et al. 2001; Bodor et al. 2005) and autoradiographic (Herkenham et al.”
BackgroundResultGanon-Elazar, E., & Akirav, I. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1223-09.2009 · Cited by 173 · see citing works
“Indeed, the potential therapeutic value of cannabinoid modulation is underscored by the dense expression of the cannabinoid CB1 receptor in regions known to be significant for anxiety and emotional learning, particularly the basolateral amygdala (BLA) (Katona et al., 2001; Haller et al., 2002).”
BackgroundLaviolette, S. R., & Grace, A. A. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-006-6027-5 · Cited by 170 · see citing works
Endocannabinoids and traumatic brain injury
Shohami, E., Cohen‐Yeshurun, A., Magid, L., Algali, M., & Mechoulam, R. (2011) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2011.01343.x · Cited by 168 · see citing works
Patel, S., Cravatt, B. F., & Hillard, C. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300535 · Cited by 164 · see citing works
“Restraint increased the number of Fos-li cells within the BLA, whereas AM404 alone had no effect (Figure 7).”
BackgroundMethodResultInfluentialAltered affective response in marijuana smokers: An FMRI study
Gruber, S. A., Rogowska, J., & Yurgelun-Todd, D. A. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.06.019 · Cited by 162 · see citing works
“The authors conclude that CB-1 receptor activation effectively reduces the threshold at which salient sensory stimuli activate the basolateral amygdala (BLA) –CeA pathway (Katona et al., 2001).”
BackgroundThe role of the amygdala in the extinction of conditioned fear.
Barad, M., Gean, P., & Lutz, B. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.029 · Cited by 168 · see citing works
Mascagni, F., & McDonald, A. J. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02625-8 · Cited by 157 · see citing works
Patel, S., Kingsley, P. J., Mackie, K., Marnett, L. J., & Winder, D. G. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.101 · Cited by 153 · see citing works
“We focused our electrophysiological studies on the BLA given the high level of both DAGLp and CB1 receptor expression in this subregion (Katona et al, 2001).”
InfluentialCB1 receptor-deficient mice as a model for depression
Valverde, O., & Torrens, M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.031 · Cited by 153 · see citing works
Cannabinoid receptors are localized to noradrenergic axon terminals in the rat frontal cortex
Oropeza, V. C., Mackie, K., & Bockstaele, E. J. V. (2006) · Brain Research · doi:10.1016/j.brainres.2006.09.110 · Cited by 150 · see citing works
Naassïla, M., Pierrefiche, O., Ledent, C. A., & Daoust, M. (2003) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.09.002 · Cited by 150 · see citing works
Burggren, A. C., Shirazi, A., Ginder, N., & London, E. D. (2019) · The American Journal of Drug and Alcohol Abuse · doi:10.1080/00952990.2019.1634086 · Cited by 144 · see citing works
“mation, and amygdala), the cerebellum and neocortex, and are expressed widely at lower levels in other brain regions (6,40,41).”
BackgroundThe endocannabinoid system: An emotional buffer in the modulation of memory function
Morena, M., & Campolongo, P. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.010 · Cited by 143 · see citing works
“Studies examining the functions of endocannabinoid signaling in the limbic system have shown that CB1 receptors play a key role in modulating synaptic transmission (Katona et al., 2001; Tan et al., 2011) and neuronal firing (Pistis et al.”
BackgroundEmerging roles for endocannabinoids in long‐term synaptic plasticity
Gerdeman, G. L., & Lovinger, D. M. (2003) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705466 · Cited by 142 · see citing works
“Experiments testing the role of Ca2þ in LTDi of the BLA have not been reported.”
BackgroundInfluentialTrezza, V., Campolongo, P., Cassano, T., Macheda, T., Dipasquale, P., Carratù, M. R., Gaetani, S., & Cuomo, V. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1162-3 · Cited by 142 · see citing works
“produced by activated neurons, act presynaptically modulating the release of several neurotransmitters and neuropeptides that play a key role in anxiety (Hermann et al. 2002; Katona et al. 2001; Schlicker and Kathmann 2001; Tsou et al. 1998; Ameri 1999; Rodriguez de Fonseca et al. 1997).”
BackgroundEndocannabinoid System and Synaptic Plasticity: Implications for Emotional Responses
Viveros, M., Marco, E. M., Llorente, R., & López‐Gallardo, M. (2007) · Neural Plasticity · doi:10.1155/2007/52908 · Cited by 144 · see citing works
“Genetic and pharmacological approaches also support an involvement of endocannabinoids in extinction of aversive memories.”
BackgroundBraida, D., Capurro, V., Zani, A. D., Rubino, T., Viganò, D., Parolaro, D., & Sala, M. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00230.x · Cited by 141 · see citing works
“Decreased FAAH activity after salvinorin A, was only observed in amygdala, which is a brain region linked with the effects of cannabinoids on emotionally relevant behaviours (Katona et al., 2001) and where anatomical studies have reported the presence of k-opioid receptors (Mansour et al., 1994).”
Background
- 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 › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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