Polymodal activation of the endocannabinoid system in the extended amygdala
Abstract
The reason why neurons synthesize more than one endocannabinoid (eCB) and how this is involved in the regulation of synaptic plasticity in a single neuron is not known. We found that 2-arachidonoylglycerol (2-AG) and anandamide mediate different forms of plasticity in the extended amygdala of rats. Dendritic L-type Ca(2+) channels and the subsequent release of 2-AG acting on presynaptic CB1 receptors triggered retrograde short-term depression. Long-term depression was mediated by postsynaptic mGluR5-dependent release of anandamide acting on postsynaptic TRPV1 receptors. In contrast, 2-AG/CB1R-mediated retrograde signaling mediated both forms of plasticity in the striatum. These data illustrate how the eCB system can function as a polymodal signal integrator to allow the diversification of synaptic plasticity in a single neuron.
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Additional reports indicate TRPV1 expression in the bed nucleus of the stria terminalis, hippocampal dentate gyrus, and hippocampal CA1 region in postsynaptic terminals of both inhibitory and excitatory synapses.
“there are additional reports of TRPV1 expression in the bed nucleus of the stria terminalis (BNST) (Puente et al., 2011), hippocampal dentate gyrus (Canduela et al., 2015; Lee et al., 2015; Puente et al., 2015) and hippocampal CA1 region (Lee et al., 2015) in postsynaptic terminals of both inhibitory (Canduela et al., 2015; Lee et al., 2015) and excitatory synapses (Puente et al., 2011; Puente et”
From The endocannabinoid system as a target for novel anxiolytic drugs (2017) · cites this paper as Puente et al., 2011
AEA of presynaptic origin can bind presynaptic TRPV1.
“AEA of presynaptic origin could also bind presynaptic TRPV1 (Puente et al., 2011).”
From The endocannabinoid system as a target for novel anxiolytic drugs (2017) · cites this paper as Puente et al., 2011
Cites
Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis
Herman, J. P., & Cullinan, W. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10069-2 · Cited by 2,270 · see citing works
The molecular logic of endocannabinoid signalling
Piomelli, D. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1247 · Cited by 1,957 · see citing works
Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,529 · see citing works
A Role for Brain Stress Systems in Addiction
Koob, G. F. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.012 · Cited by 1,056 · see citing works
Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects
Long, J. Z., Li, W., Booker, L., Burston, J. J., Kinsey, S. G., Schlosburg, J. E., Pavón, F. J., Serrano, A., Selley, D. E., Parsons, L. H., et al. (2008) · Nature Chemical Biology · doi:10.1038/nchembio.129 · Cited by 938 · see citing works
Kreitzer, A. C., & Regehr, W. G. (2001) · Neuron · doi:10.1016/s0896-6273(01)00246-x · Cited by 873 · see citing works
Luján, R., Nusser, Z., Roberts, J. D. B., Shigemoto, R., & Somogyi, P. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01611.x · Cited by 863 · see citing works
Heterosynaptic LTD of Hippocampal GABAergic Synapses
Chevaleyre, V., & Castillo, P. E. (2003) · Neuron · doi:10.1016/s0896-6273(03)00235-6 · Cited by 647 · see citing works
Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens
Robbe, D., Köpf, M., Rémaury, A., Bockaert, J., & Manzoni, O. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.122149199 · Cited by 631 · see citing works
Self-citationAnandamide and vanilloid TRPV1 receptors
Ross, R. A. (2003) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705467 · Cited by 603 · see citing works
Endocannabinoid signaling as a synaptic circuit breaker in neurological disease
Katona, I., & Freund, T. F. (2008) · Nature Medicine · doi:10.1038/nm.f.1869 · Cited by 579 · see citing works
Cavanaugh, D. J., Chesler, A. T., Jackson, A. C., Sigal, Y. M., Yamanaka, H., Grant, R., O'Donnell, D., Nicoll, R. A., Shah, N. M., Julius, D., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.6451-10.2011 · Cited by 542 · see citing works
Molecular Composition of the Endocannabinoid System at Glutamatergic Synapses
Katona, I., Urbán, G. M., Wallace, M., Ledent, C., Jung, K.-M., Piomelli, D., Mackie, K., & Freund, T. F. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0309-06.2006 · Cited by 511 · see citing works
Kawamura, Y., Fukaya, M., Maejima, T., Yoshida, T., Miura, E., Watanabe, M., Ohno‐Shosaku, T., & Kano, M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4872-05.2006 · Cited by 489 · see citing works
Cristino, L., PETROCELLIS, L. D., Pryce, G., Baker, D., Guglielmotti, V., & Marzo, V. D. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.074 · Cited by 489 · see citing works
Endocannabinoid Signaling and Long-Term Synaptic Plasticity
Heifets, B. D., & Castillo, P. E. (2009) · Annual Review of Physiology · doi:10.1146/annurev.physiol.010908.163149 · Cited by 488 · see citing works
The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors
Marrs, W., Blankman, J. L., Horne, E. A., Thomazeau, A., Lin, Y. H., Coy, J. W., Bodor, Á. L., Muccioli, G. G., Hu, S. S., Woodruff, G., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2601 · Cited by 442 · see citing works
Self-citationTRPV1 Channels Mediate Long-Term Depression at Synapses on Hippocampal Interneurons
Gibson, H. E., Edwards, J. G., Page, R. S., Van Hook, M. J., & Kauer, J. A. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.027 · Cited by 388 · see citing works
Uchigashima, 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
Robbe, D., Alonso, G., Duchamp, F., Bockaert, J., & Manzoni, O. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00109.2001 · Cited by 367 · see citing works
Self-citationMarsch, R., Foeller, E., Rammes, G., Bunck, M., Kössl, M., Holsboer, F., Zieglgänsberger, W., Landgraf, R., Lutz, B., & Wotjak, C. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3303-06.2007 · Cited by 359 · see citing works
Postsynaptic TRPV1 triggers cell type–specific long-term depression in the nucleus accumbens
Grueter, B. A., Brasnjo, G., & Malenka, R. C. (2010) · Nature Neuroscience · doi:10.1038/nn.2685 · Cited by 353 · see citing works
Chávez, A. E., Chiu, C. Q., & Castillo, P. E. (2010) · Nature Neuroscience · doi:10.1038/nn.2684 · Cited by 351 · see citing works
Yoshida, 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
Bisogno, T., Berrendero, F., Ambrosino, G., Cebeira, M., Ramos, J. A., Fernández‐Ruíz, J., & Marzo, V. D. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0254 · Cited by 313 · see citing works
Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum
Maccarrone, M., Rossi, S., Bari, M., Chiara, V. D., Fezza, F., Musella, A., Gasperi, V., Prosperetti, C., Bernardi, G., Finazzi‐Agrò, A., et al. (2008) · Nature Neuroscience · doi:10.1038/nn2042 · Cited by 293 · see citing works
Role in Anxiety Behavior of the Endocannabinoid System in the Prefrontal Cortex
Rubino, T., Realini, N., Castiglioni, C., Guidali, C., Viganò, D., Marras, E., Petrosino, S., Perletti, G., Maccarrone, M., Marzo, V. D., et al. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm161 · Cited by 283 · see citing works
Complex interactions between mGluRs, intracellular Ca2+ stores and ion channels in neurons
Fagni, L., Chavis, P., Ango, F., & Bockaert, J. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01492-7 · Cited by 279 · see citing works
Molecular Components and Functions of the Endocannabinoid System in Mouse Prefrontal Cortex
Lafourcade, M., Elezgarai, I., Mato, S., Bakiri, Y., Grandes, P., & Manzoni, O. J. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000709 · Cited by 249 · see citing works
Self-citationMarzo, V. D., PETROCELLIS, L. D., Fezza, F., Ligresti, A., & Bisogno, T. (2002) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1054/plef.2001.0349 · Cited by 238 · see citing works
Hot flash: TRPV channels in the brain
Kauer, J. A., & Gibson, H. E. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2008.12.006 · Cited by 235 · see citing works
Marzo, V. D., Bisogno, T., & PETROCELLIS, L. D. (2001) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(00)01712-0 · Cited by 226 · see citing works
Jung, K., Mangieri, R. A., Stapleton, C. J., Kim, J., Fegley, D., Wallace, M., Mackie, K., & Piomelli, D. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.013961 · Cited by 197 · see citing works
FAAH and MAGL inhibitors: therapeutic opportunities from regulating endocannabinoid levels.
Petrosino, S., & Marzo, V. D. (2010) · PubMed · Cited by 185 · see citing works
Starowicz, K., Maione, S., Cristino, L., Palazzo, E., Marabese, I., Rossi, F., de Novellis, V., & Marzo, V. D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3258-07.2007 · Cited by 168 · see citing works
Marzo, V. D., Starowicz, K., & Cristino, L. (2008) · Current Pharmaceutical Design · doi:10.2174/138161208783330790 · Cited by 153 · see citing works
Dumont, É. C., & Williams, J. T. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0425-04.2004 · Cited by 137 · see citing works
Differential diurnal variations of anandamide and 2-arachidonoyl-glycerol levels in rat brain
Valenti, M., Vigan�, D., Casico, M. G., Rubino, T., Steardo, L., Parolaro, D., & Marzo, V. D. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-3453-5 · Cited by 135 · see citing works
Tippens, A. L., Paré, J., Langwieser, N. N., Moosmang, S., Milner, T. A., Smith, Y., & Lee, A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21567 · Cited by 112 · see citing works
Jalabert, M., Aston‐Jones, G., Herzog, É., Manzoni, O. J., & Georges, F. E. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.07.010 · Cited by 103 · see citing works
Self-citationMolecular architecture of endocannabinoid signaling at nociceptive synapses mediating analgesia
Nyilas, R., Gregg, L. C., Mackie, K., Watanabe, M., Zimmer, A., Hohmann, A. G., & Katona, I. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06751.x · Cited by 94 · see citing works
TRPV1 channels control synaptic plasticity in the developing superior colliculus
Maione, S., Cristino, L., Al, M., Georgiou, A. L., Starowicz, K., Salt, T. E., & Marzo, V. D. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.171900 · Cited by 88 · see citing works
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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 · see citing works
Massi, L., Elezgarai, I., Puente, N., Reguero, L., Grandes, P., Manzoni, O. J., & Georges, F. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2291-08.2008 · Cited by 82 · see citing works
Self-citationKarbarz, M. J., Luo, L., Chang, L., Tham, C.-S., Palmer, J. A., Wilson, S. J., Wennerholm, M. L., Brown, S. M., Scott, B. P., Apodaca, R. L., et al. (2009) · Anesthesia & Analgesia · doi:10.1213/ane.0b013e31818c7cbd · Cited by 74 · see citing works
Modulation of glutamatergic synaptic transmission in the bed nucleus of the stria terminalis
McElligott, Z. A., & Winder, D. G. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.05.022 · Cited by 72 · see citing works
Mato, S., Lafourcade, M., Robbe, D., Bakiri, Y., & Manzoni, O. J. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.04.014 · Cited by 62 · see citing works
Almási, R., Szőke, É., Bölcskei, K., Varga, A., Riedl, Z., Zoltán, S., Szolcsányi, J., & Pethö, G. (2008) · Life Sciences · doi:10.1016/j.lfs.2007.12.022 · Cited by 59 · see citing works
Puente, N., Elezgarai, I., Lafourcade, M., Reguero, L., Marsicano, G., Georges, F. E., Manzoni, O. J., & Grandes, P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008869 · Cited by 57 · see citing works
Self-citationBrain TRPV1: a depressing TR(i)P down memory lane?
Marzo, V. D., Gobbi, G., & SZALLASI, A. (2008) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2008.09.004 · Cited by 37 · see citing works
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Self-citation
- Authors
- Puente, N., Cui, Y., Lassalle, O., Lafourcade, M., Georges, F., Venance, L., Grandes, P., & Manzoni, O. J.
- Affiliations
- Inserm (FR)
- Centre National de la Recherche Scientifique (FR)
- Université de Bordeaux (FR)
- Corresponding author
- Venance, Laurent
- Grandes, Pedro
- Manzoni, Olivier J
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2011-11-06
- Volume
- 14
- Issue
- 12
- Pages
- 1542-1547
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2010864051
- Cited by
- 173
- References
- 50
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 8 · 2023: 4 · 2022: 5 · 2021: 13 · 2020: 13 · 2019: 12 · 2018: 13 · 2017: 14 · 2016: 16 · 2015: 15 · 2014: 20 · 2013: 16 · 2012: 15
- FWCI
- 11.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- endocannabinoid system, extended amygdala, 2-arachidonoylglycerol, anandamide, retrograde signaling, short-term depression, long-term depression, synaptic plasticity, CB1 receptor, L-type calcium channels, mGluR5, TRPV1, striatum
- MeSH terms
- Animals, Arachidonic Acids, Biophysics, Calcium, Calcium Channel Blockers, Chromones, Cyclohexanones, Electric Stimulation, Enzyme Inhibitors, Glycerides, Neurons, Nimodipine, Piperidines, Pyrazoles, Pyridines, Septal Nuclei, Synapses, Time Factors, Signal Transduction, Rats, Sprague-Dawley, Receptors, Metabotropic Glutamate, Patch-Clamp Techniques, Excitatory Amino Acid Antagonists, Calcium Channels, L-Type, Long-Term Synaptic Depression, Receptor, Cannabinoid, CB2, TRPV Cation Channels, Rats, Cannabinoid Receptor Modulators, Endocannabinoids, Receptor, Metabotropic Glutamate 5, In Vitro Techniques
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