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Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons
Abstract
The neuronal localization of the CB1 cannabinoid receptor in the rat basolateral amygdala was studied using peroxidase and fluorescence immunohistochemical techniques. All nuclei of the basolateral amygdala contained a large number of lightly stained pyramidal neurons and a small number of more intensely stained non-pyramidal neurons. Most of the latter cells had medium-sized to large multipolar somata and three to four aspiny dendrites, but some exhibited smaller oval somata. The axon initial segments of some of these non-pyramidal neurons exhibited large swollen varicosities in colchicine-injected animals, suggesting that much of the CB1 receptor protein is transported down the axons of these cells. Double-labeling studies using immunofluorescence histochemistry combined with confocal laser scanning microscopy revealed that the great majority of non-pyramidal neurons with CB1 receptor immunoreactivity belonged to a cholecystokinin-containing subpopulation. Whereas none of the other subpopulations of non-pyramidal neurons (exhibiting immunoreactivity for calretinin, parvalbumin, or somatostatin) expressed high levels of CB1 receptor immunoreactivity, a small percentage of these cells exhibited low levels of immunoreactivity. The results indicate that cannabinoids may modulate the activity of pyramidal projection neurons as well as a subpopulation of cholecystokinin-containing non-pyramidal neurons in the basolateral amygdala. Previous studies indicate that most of the latter are inhibitory interneurons that utilize GABA as a neurotransmitter. The intense staining of the cholecystokinin-containing interneurons and the evidence that large amounts of CB1 receptor protein are transported down the axons of these cells suggests that, as in the hippocampus, cannabinoids may inhibit the release of GABA from the axon terminals of these neurons.
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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 [21]
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ENDOCANNABINOID-MEDIATED SYNAPTIC PLASTICITY IN THE CNS
Chevaleyre, V., Takahashi, K. A., & Castillo, P. E. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112834 · Cited by 829
Distribution of cannabinoid receptors in the central and peripheral nervous system
Mackie, K. (2005) · Handbook of Experimental Pharmacology · doi:10.1007/3-540-26573-2_10 · Cited by 744
“As in other regions of the forebrain, CB1 receptors are primarily expressed on large, GABAergic, CCK-containing axon terminals (Katona et al. 2001; McDonald and Mascagni 2001).”
BackgroundMolecular mechanisms underlying emotional learning and memory in the lateral amygdala
Rodrigues, S. M., Schafe, G. E., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.014 · Cited by 491
Patel, S., & Hillard, C. J. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.101287 · Cited by 397
“…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 behavior.”
BackgroundEnhancing 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
“These hybridization results are in close agreement with previous studies using immunohistochemical and hybridization techniques (Katona et al, 1999; Marsicano and Lutz, 1999; McDonald and Mascagni, 2001).”
ResultHill, M. N., & Tasker, J. G. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.12.030 · Cited by 346
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
“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 333
“, 2005), cannabinoids (Katona et al., 2001; McDonald and Mascagni, 2001; Marsicano et al., 2002) and dopamine (Brinley-Reed and McDonald, 1999; Bissiere et al.”
BackgroundHill, 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
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
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 264
“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).”
Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction
Sharp, B. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.161 · Cited by 244
Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety
Shekhar, A., Truitt, W., Rainnie, D., & Sajdyk, T. (2005) · Stress · doi:10.1080/10253890500504557 · Cited by 237
“It appears that in the BLA, similar to the cortex, the non-pyramidal cells impinge on the pyramidal cells and modulate the activity of these projection neurons (McDonald and Mascagni 2001a,b,c).”
BackgroundAmygdala 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
Azad, S. C., Eder, M., Marsicano, G., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2003) · Learning & Memory · doi:10.1101/lm.53303 · Cited by 220
“Among other brain regions, CB1 is highly expressed in the amygdala (Marsicano and Lutz 1999; Katona et al. 2001; McDonald and Mascagni 2001), which is an integral component of the limbic circuitry.”
BackgroundEndocannabinoids in the regulation of appetite and body weight
Kirkham, T. C. (2005) · Behavioural Pharmacology · doi:10.1097/00008877-200509000-00004 · Cited by 224
“CB1 receptors are also expressed by CCKcontaining neurons within the brain (McDonald and Mascagni, 2001), although the implications of this association to feeding have not been studied.”
BackgroundInterneurons in the basolateral amygdala
Spampanato, J. G., Polepalli, J. S., & Sah, P. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.11.006 · Cited by 216
“Calbindin (CB) expression accounts for approximately half of all the interneurons in the BLA and calretinin (CR) expression accounts for approximately 20% of those remaining (Kemppainen and Pitkanen, 2000; McDonald and Mascagni, 2001a).”
BackgroundLaviolette, S. R., & Grace, A. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0707-06.2006 · Cited by 189
“Receptors for endogenous cannabinoids are found ubiquitously throughout the CNS, with the CB1 cannabinoid receptor subtype localized to regions known to be involved in associative learning and emotional processing, such as the hippocampus, amygdala, striatum, and frontal cortical regions (Tsou et al., 1998; Marsicano…”
The 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 188
“Several studies have found no overlap between astrocytic and CB1 immunostaining (McDonald and Mascagni, 2001; Marchalant et al., 2007; Marchalant et al., 2008), therefore there was a call for more definitive studies to confirm that the CB1-positive perivascular glia reported by several other groups…”
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 192
“CR interneurons make up about 25–30% of BLA GABAergic interneurons and innervate primarily other interneurons (McDonald and Mascagni, 2001a; Muller et al., 2003, 2006; Capogna, 2014).”
InfluentialGanon-Elazar, E., & Akirav, I. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1223-09.2009 · Cited by 173
“Within the BLA, high concentrations of CB1 receptors are found localized on a subpopulation of inhibitory interneurons (McDonald and Mascagni, 2001), suggesting an important regulatory role for CB1 receptor transmission within the BLA through endocannabinoid signaling.”
BackgroundLaviolette, S. R., & Grace, A. A. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-006-6027-5 · Cited by 172
Patel, S., Cravatt, B. F., & Hillard, C. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300535 · Cited by 164
“CB1 receptors are also expressed by BLA pyramidal neurons, but at lower levels (McDonald and Mascagni, 2001).”
BackgroundInfluentialThe 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
Mascagni, F., & McDonald, A. J. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02625-8 · Cited by 157
Rainnie, D. G., Mania, I., Mascagni, F., & McDonald, A. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21049 · Cited by 151
Distinct cannabinoid sensitive receptors regulate hippocampal excitation and inhibition
Hájos, N., & Freund, T. F. (2002) · Chemistry and Physics of Lipids · doi:10.1016/s0009-3084(02)00149-4 · Cited by 122
Jiang, B., Huang, S., Pasquale, R. D., Millman, D. J., Song, L., Lee, H., Tsumoto, T., & Kirkwood, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.021 · Cited by 123
“…first to report endocannabinoid modulation of synaptic function made by FS-PV interneurons in the mammalian cortex, although such modulation has been documented in the amygdala (McDonald and Mascagni, 2001) and basal ganglia (Freiman et al., 2006; Narushima et al., 2006; Uchigashima et al., 2007).”
BackgroundPistis, M., Perra, S., Pillolla, G., Melis, M., Gessa, G., & Muntoni, A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.08.003 · Cited by 124
Osei‐Hyiaman, D., DePetrillo, M. A., Harvey-White, J. D., Bannon, A. W., Cravatt, B. F., Kuhar, M. J., Mackie, K., Palkovits, M., & Kunos, G. (2005) · Neuroendocrinology · doi:10.1159/000087925 · Cited by 110
Gadd, C. A., Murtra, P., Felipe, C. D., & Hunt, S. P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08271.2003 · Cited by 107
“Interestingly, the CB1 cannabinoid receptor is also expressed on the GABAergic interneurons of the basolateral nucleus, at least in the rat and the mouse (Katona et al., 2001; McDonald and Mascagni, 2001).”
BackgroundMuller, J. F., Mascagni, F., & McDonald, A. J. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10435 · Cited by 101
Lorenzetti, V., Solowij, N., Fornito, A., Lubman, D. I., & Yücel, M. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113199990435 · Cited by 99
“, including the hippocampus, amygdala, PFC and cerebellum) high in CB1 receptors [47-56] and mediating emotional [57-65] and neurocognitive processes that are altered with regular cannabinoid exposure [6, 66-77].”
BackgroundMuller, J. F., Mascagni, F., & McDonald, A. J. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21486 · Cited by 93
“…by Dr. Kenneth Baimbridge, University of British Columbia) or rabbit anti-VIP (1:2,000; Immunostar) to label specific populations of interneurons (McDonald and Mascagni, 2001a; Mascagni and McDonald, 2003), or in mouse anti-CaMK (20 g/ml; Chemicon) to label pyramidal cells (McDonald et al.,…”
InfluentialMarsicano, G., & Kuner, R. (2007) · Springer eBooks · doi:10.1007/978-0-387-74349-3_10 · Cited by 103
Tan, H., Lauzon, N. M., Bishop, S. F., Chi, N., Bechard, M., & Laviolette, S. R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4718-10.2011 · Cited by 92
“Within the BLA, high concentrations of CB1 receptors are found localized on inhibitory interneurons (McDonald and Mascagni, 2001).”
BackgroundInserra, A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00330 · Cited by 91
“Since CB1 receptors are enriched in the amygdala (one of the brain areas hyperactivated by Ayahuasca), and given that CB1 or NMDA agonists prevent fear expression during traumatic memory retrieval, this supports a role for Ayahuasca in the updating and reconsolidation of traumatic memories by modulating the fear respo…”
BackgroundInfluentialInfusion of cannabidiol into infralimbic cortex facilitates fear extinction via CB1 receptors
Monte, F. H. D., de Souza, R. R., de Bitencourt, R. M., Kroon, J. A. V., & Takahashi, R. N. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.045 · Cited by 94
Kamprath, K., Romo-Parra, H., Häring, M., Gaburro, S., Doengi, M., Lutz, B., & Pape, H.-C. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.196 · Cited by 86
“In line with this finding, other studies detected a faint immunopositive signal in the CeA (Tsou et al, 1998; McDonald and Mascagni, 2001; Patel et al, 2005a).”
ResultThe endocannabinoid system and nondrug rewarding behaviours
Fattore, L., Melis, M., Fadda, P., Pistis, M., & Fratta, W. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.03.020 · Cited by 96
“The BLA expresses high levels of CB1 receptors (Herkenham et al., 1991; Katona et al., 2001; McDonald and Mascagni, 2001) and CB1 mRNA (Marsicano and Lutz, 1999).”
BackgroundEndocannabinoids, cannabinoids and the regulation of anxiety
Petrie, G. N., Nastase, A. S., Aukema, R. J., & Hill, M. N. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108626 · Cited by 91
Falenski, K. W., Carter, D. S., Harrison, A. J., Martin, B. R., Blair, R. E., & DeLorenzo, R. J. (2009) · Brain Research · doi:10.1016/j.brainres.2009.01.036 · Cited by 85
Chapter 5 The Endocannabinoid System as A Target for Novel Anxiolytic and Antidepressant Drugs
Gaetani, S., Dipasquale, P., Romano, A., Righetti, L., Cassano, T., Piomelli, D., & Cuomo, V. (2009) · International Review of Neurobiology · doi:10.1016/s0074-7742(09)85005-8 · Cited by 83
“High densities of CB1 are found in the basolateral amygdala, the anterior cingulate cortex, the prefrontal cortex, and the hippocampus, brain regions that serve diVerent functions in the regulation of emotions (Cahill and McGaugh, 1998; McDonald and Mascagni, 2001).”
BackgroundRoberto, M., Cruz, M. T., Bajo, M., Siggins, G. R., Parsons, L. H., & Schweitzer, P. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.70 · Cited by 85
“Our data are in agreement with immunohistochemical findings of light CB1 staining in CeA (Tsou et al., 1998; McDonald and Mascagni, 2001), and apparent low levels of CB1 appear to be sufficient to generate a large physiological response.”
InfluentialSerrano, A., Rivera, P., Pavón, F. J., Decara, J. M., Suárez, J., de Fonseca, F. R., & Parsons, L. H. (2011) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01686.x · Cited by 86
“However, other studies have detected faint but consistent immunopositive CB1 signal in the CeA (Kamprath et al., 2011; McDonald and Mascagni, 2001; Patel et al., 2005a; Tsou et al., 1998) and recent work has demonstrated a robust endocannabinoid influence on both excitatory and inhibitory transmission in the CeA (Kamp…”
BackgroundGABAergic cell type diversity in the basolateral amygdala
Capogna, M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.01.006 · Cited by 91
“Another cell population that expresses cholecystokinin (CCK), often together with CB and type 1 cannabinoid (CB1) receptors [27] makes synapses with somata [28], suggesting analogy with cortical CCK-expressing basket cells [29].”
Tan, H., Lauzon, N. M., Bishop, S. F., Bechard, M. A., & Laviolette, S. R. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp210 · Cited by 81
“found localized on a subpopulation of inhibitory interneurons (McDonald and Mascagni 2001) suggesting an important regulatory role for CB1 receptor transmission within the BLA through endocannabinoid signaling.”
BackgroundInfluentialChhatwal, J. P., Gutman, A. R., Maguschak, K. A., Bowser, M. E., Yang, Y., Davis, M., & Ressler, K. J. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.97 · Cited by 80
“In terms of understanding the neural circuitry underlying the process of extinction learning, the present study in combination with the aforementioned anatomical studies describing high concentrations of CB1Rs on the presynaptic terminals of CCK + interneurons (Marsicano and Lutz, 1999; McDonald and Mascagni, 2001) su…”
BackgroundResultSupraspinal modulation of pain by cannabinoids: the role of GABA and glutamate
Rea, K., Roche, M., & Finn, D. P. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707440 · Cited by 81
Endocannabinoids: Effectors of glucocorticoid signaling
Balsevich, G., Petrie, G. N., & Hill, M. N. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.07.005 · Cited by 82
“Within the amygdala, CB1 receptors are located on both glutamatergic and GABAergic terminals (Katona et al., 2001; Marsicano and Lutz, 1999; McDonald and Mascagni, 2001), yet CB1-mediated suppression of glutamate transmission dominates, resulting in an overall reduction in the firing activity of…”
BackgroundRole of the basolateral nucleus of the amygdala in endocannabinoid-mediated stress-induced analgesia
Connell, K., Bolton, N., Olsen, D., Piomelli, D., & Hohmann, A. G. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.12.008 · Cited by 76
Functional neuroanatomy of the basolateral amygdala: Neurons, neurotransmitters, and circuits
McDonald, A. J. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00001-5 · Cited by 84
Summers, C. H., Yaeger, J. D. W., Staton, C. D., Arendt, D. H., & Summers, T. R. (2018) · Brain Research · doi:10.1016/j.brainres.2018.12.036 · Cited by 76
“Local inhibitory circuits associated with the intercalated cells and basolateral amygdala appear to play an important role regulating fear learning and extinction (Amano et al., 2010; Likhtik et al., 2008; McDonald and Mascagni, 2001; Trouche et al., 2013).”
Tan, H., Ahmad, T., Loureiro, M., Zunder, J. S., & Laviolette, S. R. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00073 · Cited by 72
Harkany, T., Härtig, W., Berghuis, P., Dobszay, M. B., Zilberter, Y., Edwards, R. H., Mackie, K., & Ernfors, P. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02898.x · Cited by 72
Huang, Y.-C., Wang, S., Chiou, L., & Gean, P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10311.2003 · Cited by 70
“Although pyramidal cells exhibited weak expression of CB1 receptor mRNA and much less CB1immunoreactive boutons ( McDonald and Mascagni, 2002 ), our results show that endocannabinoids released by amphetamine are capable of inducing LTD of excitatory synaptic transmission.”
BackgroundResultNeuronal diversity of the amygdala and the bed nucleus of the stria terminalis
Beyeler, A., & Dabrowska, J. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00003-9 · Cited by 74
Post‐natal development of type 1 cannabinoid receptor immunoreactivity in the rat hippocampus
Morozov, Y. M., & Freund, T. F. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02852.x · Cited by 67
Stress disrupts engram ensembles in lateral amygdala to generalize threat memory in mice
Lesuis, S. L., Park, S., Hoorn, A., Rashid, A. J., Mocle, A. J., Salter, E. W., Vislavski, S., Gray, M. T., Torelli, A. M., Cristofaro, A. D., et al. (2024) · Cell · doi:10.1016/j.cell.2024.10.034 · Cited by 82
“Consistent with previous reports, 77,78 we confirmed Cnr1 expression in several brain regions, including the basal nucleus of the amygdala, cortex, CA1, CA2, CA3, and dentate gyrus subfields of the dorsal hippocampus, as well as the LA (Figures 5A and 5B).”
Interneuron Types and Their Circuits in the Basolateral Amygdala
Hájos, N. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.687257 · Cited by 66
“SST interneurons have smooth or sparsely spiny dendrites, give rise to dense local axonal arborization (Vereczki et al., 2021) and often express Calb and/or neuropeptide Y (McDonald, 1989; McDonald and Mascagni, 2002) but lack nNOS (Vereczki et al., 2021).”
BackgroundAlvarez‐Jaimes, L., Polis, I. Y., & Parsons, L. H. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301630 · Cited by 64
“Overall, little is known regarding to the role of CB1 receptors in the PFC, NAC, and BLA in the modulation of drug-seeking behavior.”
BackgroundRamikie, T. S., & Patel, S. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.037 · Cited by 62
“…sized CCK neurons (type L) co-expresses CB1 (100% co-expression of CB1 and CCK in L-type CCK-positive neurons), whereas only a small population of the small CCK-expressing neurons (type S) co-expresses CB1 (10–14% co-localization depending on anatomical subregion) (McDonald and Mascagni, 2001).”
Maldonado, R. J., & Valverde, O. (2003) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2003.08.001 · Cited by 62
Mascagni, F., & McDonald, A. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.044 · Cited by 61
Jasnow, A. M., Ressler, K. J., Hammack, S. E., Chhatwal, J. P., & Rainnie, D. G. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91149.2008 · Cited by 60
“In light of the fact that CB1 receptors are expressed predominantly by CCK interneurons in the BLA (Katona et al. 2001; McDonald and Mascagni 2001b), these data would further suggest that Type I and Type II CCK interneurons may preferentially express CB1 receptors.”
BackgroundInfluentialBowers, M. E., & Ressler, K. J. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.225 · Cited by 54
“Intriguingly, Cnr1 shows a high degree of colocalization with CCK in the BLA at the mRNA and protein level (McDonald and Mascagni, 2001; Chhatwal et al, 2009).”
McDonald, A. J., & Mascagni, F. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20101 · Cited by 53
Morales, M., Wang, S., Dı́az-Ruiz, O., & Jho, D. H. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10968 · Cited by 54
“…CB1 protein were shown to be present in GABAergic neurons distributed in different areas of the telencephalon, such as cortical areas, hippocampus, dentate gyrus, and amygdala (Katona et al., 1999, 2001; Marsicano and Lutz, 1999; Tsou et al., 1999; Hajos et al., 2000; McDonald and Mascagni, 2001).”
BackgroundCox, D. J., Racca, C., & LeBeau, F. E. N. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21758 · Cited by 53
“Anti-cholecystokinin antibody preadsorption with CCK-8 (25 g/ml) abolished all immunostaining in rat basolateral amygdala (McDonald and Mascagni, 2001).”
BackgroundChegini, H., Nasehi, M., & Zarrindast, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.12.007 · Cited by 52
Perra, S., Pillolla, G., Luchicchi, A., & Pistis, M. (2008) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2007.00588.x · Cited by 49
Malikowska‐Racia, N., & Sałat, K. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.02.001 · Cited by 50
Mascagni, F., Muly, E. C., Rainnie, D. G., & McDonald, A. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.11.017 · Cited by 47
Hill, M. N., & Gorzalka, B. B. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.11.010 · Cited by 49
Sink, K. S., Segovia, K. N., Collins, L. E., Markus, E. J., Vemuri, K. V., Makriyannis, A., & Salamone, J. D. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.03.011 · Cited by 44
“2009) including prefrontal cortex, hippocampus and basolateral amygdala, express a moderate to high density of CB1 receptor protein (Chhatwal et al. 2008; Herkenham et al. 1991; Katona et al. 2001; McDonald and Mascagni 2001).”
BackgroundMolecular Mechanisms of Threat Learning in the Lateral Nucleus of the Amygdala
Sears, R. M., Schiff, H. C., & LeDoux, J. E. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-420170-5.00010-6 · Cited by 44
Dubreucq, S., Kambiré, S. J., Conforzi, M., Metna‐Laurent, M., Cannich, A., Gómez, E. S., Richard, É. M., Marsicano, G., & Chaouloff, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.049 · Cited by 44
Remmers, F., Lange, M. D., Hamann, M., Ruehle, S., Pape, H., & Lutz, B. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1411-5 · Cited by 44
“2015), therefore, might be CB1-positive as well (Marsicano and Lutz 1999; McDonald and Mascagni 2001) and thus are potentially rescued in GABA-CB1-RS mice.”
BackgroundHasanein, P., Parviz, M., Keshavarz, M., & Javanmardi, K. (2007) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2007.04592.x · Cited by 43
“The amygdala is a forebrain structure that has a high density of CB1 receptors; that is, the cannabinoid receptor subtype predominantly found in the central nervous system (CNS).(18,19) In addition to being a key region involved in the modulation of emotional and defensive responses, the amygdala is also associated wi…”
BackgroundRostkowski, A. B., Teppen, T. L., Peterson, D. A., & Urban, J. H. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22143 · Cited by 43
“…based on colocalization of GABA with different calcium-binding proteins (CaBP; calretinin, CR; parvalbumin, PV; calbindin, CB) and neuropeptides (cholecystokinin, CCK; somatostatin, SOM; neuropeptide Y, NPY) (McDonald, 1985, 1997; Kemppainen and Pitkanen, 2000; McDonald and Mascagni, 2001a).”
BackgroundMethodResultInfluentialOmiya, Y., Uchigashima, M., Konno, K., Yamasaki, M., Miyazaki, T., Yoshida, T., Kusumi, I., & Watanabe, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4681-14.2015 · Cited by 42
“In the BA, cells intensely expressing CB1 mRNA are known to be CCK-positive GABAergic interneurons (Marsicano and Lutz, 1999; Katona et al., 2001; McDonald and Mascagni, 2001).”
BackgroundZhang, W., & Rosenkranz, J. A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.33 · Cited by 42
Basolateral amygdala CB1 cannabinoid receptors mediate nicotine-induced place preference
Hashemizadeh, S., Sardari, M., & Rezayof, A. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.01.010 · Cited by 39
“Considering that CB1 receptors have predominantly expressed in the BLA (McDonald and Mascagni, 2001) and intra-BLA administration ofWIN 55,212-2 increased rewarding properties of a sub-threshold dose of nicotine (0.1 mg/kg), onemay suggest that cannabinoid CB1 receptors in the BLA have an important…”
BackgroundInfluentialThe endocannabinoid system in the amygdala and modulation of fear
Gunduz‐Cinar, O. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110116 · Cited by 40
“CB1Rs are mostly expressed on GABAergic INs that co-express the neuropeptide CCK in the amygdala (Katona et al., 2001; McDonald and Mascagni, 2001) and other brain regions (Bodor et al.”
Morphological and physiological properties of CCK/CB1R-expressing interneurons in the basal amygdala
Rovira-Esteban, L., Péterfi, Z., Vikór, A., Máté, Z., Szabó, G., & Hájos, N. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1417-z · Cited by 34
“These studies uncovered that the vast majority of CCK+ interneurons innervating PNs uniformly express the type 1 cannabinoid receptor (CB1R) on their boutons (Katona et al. 2001; McDonald and Mascagni 2001; Vogel et al. 2016; Barsy et al. 2016; Veres et al. 2017).”
BackgroundInfluentialNECAB1 and NECAB2 are Prevalent Calcium-Binding Proteins of CB1/CCK-Positive GABAergic Interneurons
Miczán, V., Kelemen, K., Glavinics, J. R., László, Z. I., Barti, B., Kenesei, K., Kisfali, M., & Katona, I. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa326 · Cited by 30
Ferland, J. N., Ellis, R. J., Betts, G., Silveira, M. M., de Firmino, J. B., Winstanley, C. A., & Hurd, Y. L. (2022) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2022.3915 · Cited by 32
Rovira-Esteban, L., Gunduz‐Cinar, O., Bukalo, O., Limoges, A., Brockway, E. T., Müller, K., Fenno, L. E., Kim, Y. S., Ramakrishnan, C., Andrási, T., et al. (2019) · eNeuro · doi:10.1523/eneuro.0220-19.2019 · Cited by 34
“Targeted neurons express functional CB1R Based on earlier reports that CCK-containing basket cells in the BA express CB1R, we next asked whether the targeted BA INs were CB1R-positive (Katona et al., 2001; McDonald and Mascagni, 2001a; Vereczki et al., 2016; Veres et al., 2017).”
BackgroundInfluentialInhibitory Circuits in the Basolateral Amygdala in Aversive Learning and Memory
Perumal, M. B., & Sah, P. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.633235 · Cited by 31
“Nearly half these cells also express calbindin (McDonald and Mascagni, 2002).”
BackgroundInfluentialHarkany, T., Dobszay, M. B., Cayetanot, F., Härtig, W., Siegemund, T., Aujard, F., & Mackie, K. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.06.043 · Cited by 30
Endocannabinoid signaling and memory dynamics: A synaptic perspective
Drumond, A., Madeira, N., & Fonseca, R. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.031 · Cited by 29
García‐Gutiérrez, M. S., & Manzanares, J. (2009) · Journal of Psychopharmacology · doi:10.1177/0269881109106910 · Cited by 30
“The dose of 20 mg/kg was without effects in all the brain regions examined (AMY F(3,31)¼ 28.833, p¼ 0.065; CA1 F(3,32)¼ 5.905, p¼ 0.499; CA2 F(3,33)¼ 0.764, p¼ 0.558; CA3 F(3,34)¼ 0.337, p¼ 0.815; DG F(3,30)¼ 0.074, p¼ 0.883) (Figure 2).”
BackgroundInfluentialFitzgerald, M. L., Mackie, K., & Pickel, V. M. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24704 · Cited by 28
“These findings are in agreement with the expression of CB1 in a subpopulation of CCKcontaining interneurons in the amygdala (McDonald & Mascagni, 2001), and are also consistent with findings in the mouse forebrain (Marsicano & Lutz, 1999).”
Result
Metadata
- Authors
- McDonald, A. J., & Mascagni, F.
- Affiliations
- University of South Carolina (US)
- Corresponding author
- McDonald, A.J
- ORCID
- McDonald, A.J
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2001-11
- Volume
- 107
- Issue
- 4
- Pages
- 641-652
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2034121461
- Cited by
- 157
- References
- 51
- Citations by year
- 2025: 2 · 2024: 4 · 2023: 4 · 2022: 4 · 2021: 8 · 2020: 9 · 2019: 5 · 2018: 2 · 2017: 5 · 2016: 2 · 2015: 6 · 2014: 9 · 2013: 10 · 2012: 1
- FWCI
- 4.90
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 41301, P30DK041301)
- National Institute of Neurological Disorders and Stroke (NS 38998)
- 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 › Neuropeptides and Animal Physiology
- Keywords
- CB1 receptor, basolateral amygdala, cholecystokinin, interneurons, non-pyramidal neurons, axonal transport, calretinin, parvalbumin, somatostatin
- MeSH terms
- Amygdala, Animals, Antibody Specificity, Cholecystokinin, Fluorescent Antibody Technique, Immunoenzyme Techniques, Interneurons, Male, Receptors, Drug, Rats, Sprague-Dawley, Microscopy, Confocal, Receptors, Cannabinoid, Rats
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