Multiple forms of endocannabinoid and endovanilloid signaling regulate the tonic control of GABA release
Open accessAbstract
Persistent CB1 cannabinoid receptor activity limits neurotransmitter release at various synapses throughout the brain. However, it is not fully understood how constitutively active CB1 receptors, tonic endocannabinoid signaling, and its regulation by multiple serine hydrolases contribute to the synapse-specific calibration of neurotransmitter release probability. To address this question at perisomatic and dendritic GABAergic synapses in the mouse hippocampus, we used a combination of paired whole-cell patch-clamp recording, liquid chromatography/tandem mass spectrometry, stochastic optical reconstruction microscopy super-resolution imaging, and immunogold electron microscopy. Unexpectedly, application of the CB1 antagonist and inverse agonist AM251 [N-1-(2,4-dichlorophenyl)-5-(4-iodophenyl)-4-methyl-N-1-piperidinyl-1H-pyrazole-3-carboxamide], but not the neutral antagonist NESS0327 [8-chloro-1-(2,4-dichlorophenyl)-N-piperidin-1-yl-5,6-dihydro-4H-benzo[2,3]cyclohepta[2,4-b]pyrazole-3-carboxamine], significantly increased synaptic transmission between CB1-positive perisomatic interneurons and CA1 pyramidal neurons. JZL184 (4-nitrophenyl 4-[bis(1,3-benzodioxol-5-yl)(hydroxy)methyl]piperidine-1-carboxylate), a selective inhibitor of monoacylglycerol lipase (MGL), the presynaptic degrading enzyme of the endocannabinoid 2-arachidonoylglycerol (2-AG), elicited a robust increase in 2-AG levels and concomitantly decreased GABAergic transmission. In contrast, inhibition of fatty acid amide hydrolase (FAAH) by PF3845 (N-pyridin-3-yl-4-[[3-[5-(trifluoromethyl)pyridin-2-yl]oxyphenyl]methyl]piperidine-1-carboxamide) elevated endocannabinoid/endovanilloid anandamide levels but did not change GABAergic synaptic activity. However, FAAH inhibitors attenuated tonic 2-AG increase and also decreased its synaptic effects. This antagonistic interaction required the activation of the transient receptor potential vanilloid receptor TRPV1, which was concentrated on postsynaptic intracellular membrane cisternae at perisomatic GABAergic symmetrical synapses. Interestingly, neither AM251, JZL184, nor PF3845 affected CB1-positive dendritic interneuron synapses. Together, these findings are consistent with the possibility that constitutively active CB1 receptors substantially influence perisomatic GABA release probability and indicate that the synaptic effects of tonic 2-AG release are tightly controlled by presynaptic MGL activity and also by postsynaptic endovanilloid signaling and FAAH activity. SIGNIFICANCE STATEMENT: Tonic cannabinoid signaling plays a critical role in the regulation of synaptic transmission. However, the mechanistic details of how persistent CB1 cannabinoid receptor activity inhibits neurotransmitter release have remained elusive. Therefore, electrophysiological recordings, lipid measurements, and super-resolution imaging were combined to elucidate those signaling molecules and mechanisms that underlie tonic cannabinoid signaling. The findings indicate that constitutive CB1 activity has pivotal function in the tonic control of hippocampal GABA release. Moreover, the endocannabinoid 2-arachidonoylglycerol (2-AG) is continuously generated postsynaptically, but its synaptic effect is regulated strictly by presynaptic monoacylglycerol lipase activity. Finally, anandamide signaling antagonizes tonic 2-AG signaling via activation of postsynaptic transient receptor potential vanilloid TRPV1 receptors. This unexpected mechanistic diversity may be necessary to fine-tune GABA release probability under various physiological and pathophysiological conditions.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 Lee et al., 2015
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM)
Rust, M. J., Bates, M., & Zhuang, X. (2006) · Nature Methods · doi:10.1038/nmeth929 · Cited by 8,109 · see citing works
Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide
Zygmunt, P. M., Petersson, J., Andersson, D. A., Chuang, H.-H., Sørgård, M., Di Marzo, V., Julius, D., & Högestätt, E. D. (1999) · Nature · doi:10.1038/22761 · Cited by 2,142 · see citing works
Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides
Cravatt, B. F., Giang, D. K., Mayfield, S. P., Boger, D. L., Lerner, R. A., & Gilula, N. B. (1996) · Nature · doi:10.1038/384083a0 · Cited by 2,125 · see citing works
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050 · see citing works
A second endogenous cannabinoid that modulates long-term potentiation
Stella, N., Schweitzer, P., & Piomelli, D. (1997) · Nature · doi:10.1038/42015 · Cited by 1,496 · see citing works
Brain monoglyceride lipase participating in endocannabinoid inactivation
Dinh, T. P., Carpenter, D., Leslie, F. M., Freund, T. F., Katona, I., Sensi, S. L., Kathuria, S., & Piomelli, D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152334899 · Cited by 1,373 · see citing works
Self-citationModulation of anxiety through blockade of anandamide hydrolysis
Kathuria, S., Gaetani, S., Fegley, D., Valiño, F., Duranti, A., Tontini, A., Mor, M., Tarzia, G., Rana, G. L., Calignano, A., et al. (2003) · Nature Medicine · doi:10.1038/nm803 · Cited by 1,293 · see citing works
Katona, I., Sperlágh, B., Sı́k, A., Käfalvi, A., Vizi, E. S., Mackie, K., & Freund, T. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04544.1999 · Cited by 1,218 · see citing works
Self-citationA Comprehensive Profile of Brain Enzymes that Hydrolyze the Endocannabinoid 2-Arachidonoylglycerol
Blankman, J. L., Simon, G. M., & Cravatt, B. F. (2007) · Chemistry & Biology · doi:10.1016/j.chembiol.2007.11.006 · Cited by 1,177 · see citing works
Endocannabinoid Signaling and Synaptic Function
Castillo, P. E., Younts, T. J., Chávez, A. E., & Hashimotodani, Y. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.020 · Cited by 1,126 · see citing works
Bisogno, T., Howell, F., Williams, G., Minassi, A., Cascio, M. G., Ligresti, A., Matias, I., Schiano-Moriello, A., Paul, P., Williams, E.-J., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200305129 · Cited by 1,039 · 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
Neuromodulation of neuronal circuits: back to the future
Marder, E. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.010 · Cited by 904 · see citing works
Superresolution Imaging of Chemical Synapses in the Brain
Dani, A., Huang, B., Bergan, J. F., Dulac, C. G., & Zhuang, X. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.021 · Cited by 718 · see citing works
Extrasynaptic GABAA Receptors: Their Function in the CNS and Implications for Disease
Brickley, S. G., & Módy, I. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.012 · Cited by 674 · see citing works
Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system
Schlosburg, J. E., Blankman, J. L., Long, J. Z., Nomura, D. K., Pan, B., Kinsey, S. G., Nguyen, P. T., Ramesh, D., Booker, L., Burston, J. J., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2616 · Cited by 641 · see citing works
Multiple Functions of Endocannabinoid Signaling in the Brain
Katona, I., & Freund, T. F. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150420 · Cited by 630 · see citing works
Self-citationGulyas, A. I., Cravatt, B. F., Bracey, M. H., Dinh, T. P., Piomelli, D., Boscia, F., & Freund, T. F. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03428.x · Cited by 561 · see citing works
Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons
Twitchell, W., Brown, S., & Mackie, K. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.1.43 · Cited by 544 · 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
Self-citationBouaboula, M., Perachon, S., Milligan, L., Canat, X., Rinaldi, M. L., Portier, M., Barth, F., Calandra, B., Pecceu, F., Lupker, J. H., et al. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.35.22330 · Cited by 461 · see citing works
The probability of neurotransmitter release: variability and feedback control at single synapses
Branco, T., & Staras, K. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2634 · Cited by 445 · see citing works
Inverse agonism and neutral antagonism at cannabinoid CB1 receptors
Pertwee, R. G. (2004) · Life Sciences · doi:10.1016/j.lfs.2004.10.025 · Cited by 444 · see citing works
Discovery and Characterization of a Highly Selective FAAH Inhibitor that Reduces Inflammatory Pain
Ahn, K., Johnson, D. S., Mileni, M., Beidler, D., Long, J. Z., McKinney, M. K., Weerapana, E., Sadagopan, N., Liimatta, M., Smith, S. E., et al. (2009) · Chemistry & Biology · doi:10.1016/j.chembiol.2009.02.013 · Cited by 439 · see citing works
Principles: Receptor theory in pharmacology
Kenakin, T. (2004) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2004.02.012 · Cited by 412 · see citing works
Mechanisms of Cannabinoid Inhibition of GABAASynaptic Transmission in the Hippocampus
Hoffman, A. F., & Lupica, C. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02470.2000 · Cited by 401 · see citing works
Long, J. Z., Nomura, D. K., Vann, R. E., Walentiny, D. M., Booker, L., Jin, X., Burston, J. J., Sim‐Selley, L. J., Lichtman, A. H., Wiley, J. L., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909411106 · Cited by 393 · see citing works
Gavva, N. R., Tamir, R., Qu, Y., Klionsky, L., Zhang, T. J., Immke, D. C., Wang, L., Zhu, D., Vanderah, T. W., Porreca, F., et al. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.104.079855 · Cited by 390 · see citing works
Marsch, 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
Parvalbumin-Positive Basket Cells Differentiate among Hippocampal Pyramidal Cells
Lee, S.-H., Marchionni, I., Bezaire, M., Varga, C., Danielson, N., Lovett-Barron, M., Losonczy, A., & Soltesz, I. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.034 · Cited by 358 · see citing works
Self-citationPeripheral Cannabinoid-1 Receptor Inverse Agonism Reduces Obesity by Reversing Leptin Resistance
Tam, J., Çınar, R., Liu, J., Godlewski, G., Wesley, D., Jourdan, T., Szanda, G., Mukhopadhyay, B., Chedester, L., Liow, J., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.07.002 · Cited by 356 · 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
Egertová, M., Giang, D. K., Cravatt, B. F., & Elphick, M. R. (1998) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1998.0543 · Cited by 333 · 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
Self-citationChemical Probes of Endocannabinoid Metabolism
Blankman, J. L., & Cravatt, B. F. (2013) · Pharmacological Reviews · doi:10.1124/pr.112.006387 · Cited by 327 · 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
Why do cannabinoid receptors have more than one endogenous ligand?
Di Marzo, V., & De Petrocellis, L. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2011.0382 · Cited by 290 · see citing works
FAAH genetic variation enhances fronto-amygdala function in mouse and human
Dincheva, I., Drysdale, A. T., Hartley, C. A., Johnson, D. C., Jing, D., King, E. C., Ra, S., Gray, J. M., Yang, R., DeGruccio, A. M., et al. (2015) · Nature Communications · doi:10.1038/ncomms7395 · Cited by 289 · see citing works
Huang, G. Z., & Woolley, C. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.035 · Cited by 288 · see citing works
Autism-Associated Neuroligin-3 Mutations Commonly Disrupt Tonic Endocannabinoid Signaling
Földy, C., Malenka, R. C., & Südhof, T. C. (2013) · Neuron · doi:10.1016/j.neuron.2013.02.036 · Cited by 287 · 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 · cited 2× · see citing works
“, 2009a), emerging evidence indicates that specific forms of phasic and tonic endocannabinoid signaling at given brain circuit locations or under specific physiological conditions are mediated by anandamide (Azad et al., 2004; Kim and Alger, 2010; Huang and Woolley, 2012; Lerner and Kreitzer, 2012; Khlaifia et al., 20…”
BackgroundPawelzik, H., Hughes, D. I., & Thomson, A. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10118 · Cited by 262 · see citing works
Hillard, C. J. (2000) · Prostaglandins & Other Lipid Mediators · doi:10.1016/s0090-6980(00)00051-4 · Cited by 255 · see citing works
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
Endocannabinoid-mediated retrograde modulation of synaptic transmission
Ohno‐Shosaku, T., & Kano, M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.03.017 · Cited by 244 · see citing works
Ludányi, A., Erőss, L., Czirják, S., Vajda, J., Halász, P., Watanabe, M., Palkovits, M., Maglóczky, Z., Freund, T. F., & Katona, I. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4465-07.2008 · Cited by 241 · see citing works
Self-citationFukudome, Y., Ohno‐Shosaku, T., Matsui, M., Omori, Y., Fukaya, M., Tsubokawa, H., Taketo, M. M., Watanabe, M., Manabe, T., & Kano, M. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03384.x · Cited by 238 · see citing works
Self-citationAmygdala 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
Cell-specific STORM super-resolution imaging reveals nanoscale organization of cannabinoid signaling
Dudok, B., Barna, L., Ledri, M., Szabó, S. I., Szabadits, E., Pintér, B., Woodhams, S. G., Henstridge, C. M., Balla, G. Y., Nyilas, R., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3892 · Cited by 227 · see citing works
Self-citationLong-Term Plasticity of Endocannabinoid Signaling Induced by Developmental Febrile Seizures
Chen, K., Ratzliff, A., Hilgenberg, L. G. W., Gulyás, A. I., Freund, T. F., Smith, M., Dinh, T. P., Piomelli, D., Mackie, K., & Soltész, I. (2003) · Neuron · doi:10.1016/s0896-6273(03)00499-9 · Cited by 204 · see citing works
Leterrier, C., Lainé, J., Darmon, M. C., Boudin, H., Rossier, J., & Lenkei, Z. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5437-05.2006 · Cited by 201 · see citing works
Vida, I., Halasy, K., Szinyei, C., Somogyi, P., & Buhl, E. H. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.755bv.x · Cited by 190 · see citing works
Neu, A. D., Földy, C., & Soltész, I. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.115691 · Cited by 186 · see citing works
Hashimotodani, Y., Ohno‐Shosaku, T., & Kano, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4159-06.2007 · Cited by 186 · see citing works
Pan, X., Ikeda, S. R., & Lewis, D. L. (1998) · Molecular Pharmacology · doi:10.1124/mol.54.6.1064 · Cited by 186 · see citing works
Lerner, T. N., & Kreitzer, A. C. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.015 · Cited by 185 · see citing works
Endocannabinoid signalling: has it got rhythm?
Vaughn, L. K., Denning, G., Stuhr, K. L., de Wit, H., Hill, M. N., & Hillard, C. J. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00790.x · Cited by 176 · see citing works
Polymodal activation of the endocannabinoid system in the extended amygdala
Puente, N., Cui, Y., Lassalle, O., Lafourcade, M., Georges, F., Venance, L., Grandes, P., & Manzoni, O. J. (2011) · Nature Neuroscience · doi:10.1038/nn.2974 · Cited by 173 · see citing works
Sullivan, J. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.3.1286 · Cited by 173 · see citing works
Nyíri, G., Cserép, C., Szabadits, E., Mackie, K., & Freund, T. F. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.026 · Cited by 162 · see citing works
Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons
Losonczy, A., Biró, Á. A., & Nusser, Z. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0304752101 · Cited by 161 · see citing works
Antistress Effect of TRPV1 Channel on Synaptic Plasticity and Spatial Memory
Li, H.-B., Mao, R., Zhang, J., Yang, Y., Cao, J., & Xu, L. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.02.020 · Cited by 160 · see citing works
Monoacylglycerols Activate TRPV1 – A Link between Phospholipase C and TRPV1
Zygmunt, P. M., Ermund, A., Movahed, P., Andersson, D. A., Simonsen, C., Jönsson, B., Blomgren, A., Birnir, B., Bevan, S., Eschalier, A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081618 · Cited by 157 · see citing works
Chen, K., Neu, A. D., Howard, A. L., Földy, C., Echegoyen, J. C., Hilgenberg, L. G. W., Smith, M. J., Mackie, K., & Soltész, I. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3966-06.2007 · Cited by 156 · see citing works
Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses
Kim, J., & Alger, B. E. (2010) · Nature Neuroscience · doi:10.1038/nn.2517 · Cited by 149 · see citing works
Pan, B., Wang, W., Zhong, P., Blankman, J. L., Cravatt, B. F., & Liu, Q.-S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2075-11.2011 · Cited by 147 · see citing works
Cope, D. W., Maccaferri, G., Márton, L. F., Roberts, J. D. B., Cobden, P. M., & Somogyi, P. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00440-7 · Cited by 144 · see citing works
Földy, C., Neu, A. D., Jones, M. V., & Soltész, I. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4587-05.2006 · Cited by 142 · see citing works
Adenosine: setting the stage for plasticity
Dias, R. B., Rombo, D. M., Ribeiro, J. A., Henley, J. M., & Sebastião, A. M. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.12.003 · Cited by 137 · see citing works
Hentges, S. T., Low, M. J., & Williams, J. T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2769-05.2005 · Cited by 136 · see citing works
More surprises lying ahead. The endocannabinoids keep us guessing
Piomelli, D. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.07.026 · Cited by 128 · see citing works
Zhu, P., & Lovinger, D. M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1148-05.2005 · Cited by 125 · see citing works
Sumislawski, J. J., Ramikie, T. S., & Patel, S. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.166 · Cited by 124 · see citing works
Niehaus, J. L., Liu, Y., Wallis, K. T., Egertová, M., Bhartur, S. G., Mukhopadhyay, S., Shi, S., He, H., Selley, D. E., Howlett, A. C., et al. (2007) · Molecular Pharmacology · doi:10.1124/mol.107.039263 · Cited by 121 · see citing works
Cristino, L., Starowicz, K., De Petrocellis, L., Morishita, J., Ueda, N., Guglielmotti, V., & Di Marzo, V. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2007.11.047 · Cited by 115 · see citing works
Lee, S.-H., Foldy, C., & Soltesz, I. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6238-09.2010 · Cited by 114 · see citing works
Self-citationMoreira, F. A., de Aguiar, D. C., Terzian, A. L. B., Guimarães, F. S., & Wotjak, C. T. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.046 · Cited by 112 · see citing works
Oliet, S. H. R., Baimoukhametova, D. V., Piet, R., & Bains, J. S. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2676-06.2007 · Cited by 107 · cited 4× · see citing works
“, 2012) and have an essential function in the tonic control of neurotransmitter release (Losonczy et al., 2004; Hentges et al., 2005; Zhu and Lovinger, 2005; Neu et al., 2007; Oliet et al., 2007).”
BackgroundInfluentialNissen, W., Szabo, A., Somogyi, J., Somogyi, P., & Lamsa, K. P. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3481-09.2010 · Cited by 105 · see citing works
Circadian rhythm of circulating levels of the endocannabinoid 2-arachidonoylglycerol
Hanlon, E. C., Tasali, E., Leproult, R., Stuhr, K. L., Doncheck, E., de Wit, H., Hillard, C. J., & Van Cauter, E. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-3455 · Cited by 101 · see citing works
Uchigashima, M., Yamazaki, M., Yamasaki, M., Tanimura, A., Sakimura, K., Kano, M., & Watanabe, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5665-10.2011 · Cited by 97 · see citing works
Self-citationRuiu, S., Pinna, G. A., Marchese, G., Mussinu, J., Saba, P., Tambaro, S., Casti, P., Vargiu, R., & Pani, L. (2003) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.049924 · Cited by 91 · see citing works
Szabo, G. G., Lenkey, N., Holderith, N. B., Andrási, T., Nusser, Z., & Hájos, N. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0247-14.2014 · Cited by 87 · see citing works
Roberto, M., Cruz, M. T., Bajo, M., Siggins, G. R., Parsons, L. H., & Schweitzer, P. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.70 · Cited by 84 · see citing works
Serrano, 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 83 · see citing works
Alger, B. E. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.220855 · Cited by 82 · see citing works
Mato, S., Pazos, Á., & Valdizán, E. M. (2002) · European Journal of Pharmacology · doi:10.1016/s0014-2999(02)01575-3 · Cited by 80 · see citing works
Neutral antagonism at the cannabinoid 1 receptor: a safer treatment for obesity
Meye, F. J., Trezza, V, Vanderschuren, L. J. M. J., Ramakers, G. M. J., & Adan, R. A. H. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.145 · Cited by 76 · see citing works
You, I., Jung, Y., Kim, M., Kwon, S., Hong, S., Lee, S., & Jang, C. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.10.013 · Cited by 73 · see citing works
Self-citationTakács, V. T., Szőnyi, A., Freund, T. F., Nyíri, G., & Gulyás, A. I. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0692-6 · Cited by 69 · see citing works
Ali, A. B., & Todorova, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07165.x · Cited by 66 · see citing works
Voltage drives diverse endocannabinoid signals to mediate striatal microcircuit-specific plasticity
Mathur, B. N., Tanahira, C., Tamamaki, N., & Lovinger, D. M. (2013) · Nature Neuroscience · doi:10.1038/nn.3478 · Cited by 60 · see citing works
Chávez, A. E., Hernández, V. M., Rodenas-Ruano, A., Chan, C. S., & Castillo, P. E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3635-14.2014 · Cited by 59 · see citing works
D’Antona, A. M., Ahn, K. H., & Kendall, D. A. (2006) · Biochemistry · doi:10.1021/bi060067k · Cited by 59 · see citing works
Thibault, K., Carrel, D., Bonnard, D., Gallatz, K., Simon, A., Biard, M., Pezet, S., Palkovits, M., & Lenkei, Z. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs240 · Cited by 59 · see citing works
Cannabinoid Receptor–Interacting Protein 1a Modulates CB1 Receptor Signaling and Regulation
Smith, T. H., Blume, L. C., Straiker, A. J., Cox, J. O., David, B. G., McVoy, J. R. S., Sayers, K. W., Poklis, J. L., Abdullah, R. A., Egertová, M., et al. (2015) · Molecular Pharmacology · doi:10.1124/mol.114.096495 · Cited by 56 · see citing works
Cannabinoid signaling in inhibitory autaptic hippocampal neurons
Straiker, A. J., & Mackie, K. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.06.004 · Cited by 52 · see citing works
Lenkey, N., Kirizs, T., Holderith, N., Máté, Z., Szabó, G., Vizi, E. S., Hájos, N., & Nusser, Z. (2015) · Nature Communications · doi:10.1038/ncomms7557 · Cited by 45 · see citing works
Changing the tune: plasticity and adaptation of retrograde signals
Iremonger, K. J., Cusulin, J. I. W., & Bains, J. S. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.04.007 · Cited by 42 · see citing works
Dvorzhak, A., Semtner, M., Faber, D. S., & Grantyn, R. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.241018 · Cited by 42 · see citing works
Musella, A., Chiara, V. D., Rossi, S., Cavasinni, F., Castelli, M., Cantarella, C., Mataluni, G., Bernardi, G., & Centonze, D. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.02.058 · Cited by 41 · see citing works
Functional diversity on synaptic plasticity mediated by endocannabinoids
Cachope, R. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0386 · Cited by 37 · see citing works
Pardini, M., Krüeger, F., Koenigs, M. R., Raymont, V., Hodgkinson, C. A., Zoubak, S., Goldman, D. A., & Grafman, J. H. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.1 · Cited by 34 · see citing works
Mutations in the ‘DRY’ motif of the CB1 cannabinoid receptor result in biased receptor variants
Gyombolai, P., Tóth, A. D., Tímár, D., Turu, G., & Hunyady, L. (2014) · Journal of Molecular Endocrinology · doi:10.1530/jme-14-0219 · Cited by 34 · see citing works
Puente, N., Reguero, L., Elezgarai, I., Canduela, M. J., Mendizabal‐Zubiaga, J., Ramos, A., Fernández‐Espejo, E., & Grandes, P. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0711-2 · Cited by 33 · see citing works
Szabo, G. G., Papp, O. I., Máté, Z., Szabó, G., & Hájos, N. (2014) · Hippocampus · doi:10.1002/hipo.22330 · Cited by 31 · see citing works
Melis, M., Greco, B., & Tonini, R. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12501 · Cited by 30 · see citing works
Activation-dependent plasticity of polarized GPCR distribution on the neuronal surface
Simon, A., Loverdo, C., Gaffuri, A.-L., Urbanski, M., Ladarré, D., Carrel, D., Rivals, I., Leterrier, C., Bénichou, O., Dournaud, P., et al. (2013) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjt014 · Cited by 29 · see citing works
Brain region‐specific changes in N‐acylethanolamine contents with time of day
Liedhegner, E. S., Sasman, A., & Hillard, C. J. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12495 · Cited by 24 · see citing works
Ladarré, D., Roland, A. B., Biedzinski, S., Ricobaraza, A., & Lenkei, Z. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00426 · Cited by 23 · see citing works
Khlaifia, A., Farah, H., Gackière, F., & Tell, F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1028-13.2013 · Cited by 20 · see citing works
Horváth, E., Woodhams, S. G., Nyilas, R., Henstridge, C. M., Kano, M., Sakimura, K., Watanabe, M., & Katona, I. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12470 · Cited by 18 · see citing works
Self-citationKallendrusch, S., Hobusch, C., Ehrlich, A., Nowicki, M., Ziebell, S., Bechmann, I., Geißlinger, G., Koch, M., & Dehghani, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051208 · Cited by 12 · see citing works
Flagged first, then by citations
1 of the 115 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · see citing works
Cannabidiol as a Potential Treatment for Anxiety Disorders
Blessing, E., Steenkamp, M. M., Manzanares, J., & Marmar, C. R. (2015) · Neurotherapeutics · doi:10.1007/s13311-015-0387-1 · Cited by 718 · see citing works
Ligresti, A., PETROCELLIS, L. D., & Marzo, V. D. (2016) · Physiological Reviews · doi:10.1152/physrev.00002.2016 · Cited by 484 · see citing works
CB1 Receptor Signaling in the Brain: Extracting Specificity from Ubiquity
Busquets-García, A., Bains, J. S., & Marsicano, G. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.206 · Cited by 341 · see citing works
The cannabinoid system and pain
Woodhams, S. G., Chapman, V., Finn, D. P., Hohmann, A. G., & Neugebauer, V. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.06.015 · Cited by 272 · see citing works
The endocannabinoid system as a target for novel anxiolytic drugs
Patel, S., Hill, M. N., Cheer, J. F., Wotjak, C. T., & Holmes, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.033 · Cited by 233 · see citing works
Cannabinoid Control of Learning and Memory through HCN Channels
Maroso, M., Szabo, G. G., Kim, H. K., Alexander, A., Bui, A. D., Lee, S.-H., Lutz, B., & Soltész, I. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.023 · Cited by 186 · see citing works
Self-citationDon't Worry, Be Happy: Endocannabinoids and Cannabis at the Intersection of Stress and Reward
Volkow, N. D., Hampson, A. J., & Baler, R. (2016) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010716-104615 · Cited by 150 · see citing works
Hippocampal GABAergic interneurons and memory
Tzilivaki, A., Tukker, J. J., Maier, N., Poirazi, P., Sammons, R. P., & Schmitz, D. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.016 · Cited by 145 · see citing works
The GABAergic Hypothesis for Cognitive Disabilities in Down Syndrome
Contestabile, A., Magara, S., & Cancedda, L. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00054 · Cited by 141 · see citing works
The Endocannabinoid Signaling System in the CNS
Hillard, C. J. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.10.001 · Cited by 135 · see citing works
Cannabis: A Treasure Trove or Pandora's Box?
Solymosi, K., & Köfalvi, A. (2016) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557516666161004162133 · Cited by 88 · see citing works
Reviewing the Role of the Endocannabinoid System in the Pathophysiology of Depression
Gallego‐Landin, I., García-Baos, A., Castro‐Zavala, A., & Valverde, O. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.762738 · Cited by 84 · see citing works
Farkas, I., Vastagh, C., Farkas, E., Bálint, F., Skrapits, K., Hrabovszky, E., Fekete, C., & Liposits, Z. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00214 · Cited by 79 · see citing works
Richards, J. R., Lapoint, J. M., & Putze, G. B. (2017) · Clinical Toxicology · doi:10.1080/15563650.2017.1349910 · Cited by 80 · see citing works
Smith, D. R., Stanley, C. M., Foss, T., Boles, R. G., & McKernan, K. J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0187926 · Cited by 77 · see citing works
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 78 · see citing works
Cannabinoid receptor type-1: breaking the dogmas
Busquets-García, A., Gómez, E. S., Bellocchio, L., & Marsicano, G. (2016) · F1000Research · doi:10.12688/f1000research.8245.1 · Cited by 74 · see citing works
Correlated confocal and super-resolution imaging by VividSTORM
Barna, L., Dudok, B., Miczán, V., Horváth, A., László, Z. I., & Katona, I. (2015) · Nature Protocols · doi:10.1038/nprot.2016.002 · Cited by 73 · see citing works
Self-citationAuthement, M. E., Langlois, L. D., Shepard, R. D., Browne, C. A., Lucki, I., Kassis, H., & Nugent, F. S. (2018) · Science Signaling · doi:10.1126/scisignal.aan6480 · Cited by 69 · see citing works
Space–brain: The negative effects of space exposure on the central nervous system
Limoli, C., Jandial, R., Hoshide, R., & Waters, J. (2018) · Surgical Neurology International · doi:10.4103/sni.sni_250_17 · Cited by 66 · see citing works
Self-citationGomis‐González, M., Busquets-García, A., Matute, C., Maldonado, R. J., Mato, S., & Ozaita, A. (2016) · Genes · doi:10.3390/genes7090056 · Cited by 61 · see citing works
Mechanisms of endocannabinoid control of synaptic plasticity
Winters, B. L., & Vaughan, C. W. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108736 · Cited by 63 · see citing works
Bialecki, J., Werner, A. C., Weilinger, N. L., Tucker, C. M., Vecchiarelli, H. A., Huguet, J. E., Mendizabal‐Zubiaga, J., Grandes, P., Hill, M. N., & Thompson, R. J. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0257-19.2019 · Cited by 57 · see citing works
Retrograde endocannabinoid signaling at inhibitory synapses in vivo
Dudok, B., Fan, L. Z., Farrell, J. S., Malhotra, S., Homidan, J., Kim, D. K., Wenardy, C., Ramakrishnan, C., Li, Y., Deisseroth, K. A., et al. (2024) · Science · doi:10.1126/science.adk3863 · Cited by 57 · see citing works
Self-citationCyclooxygenase-2 inhibition reduces stress-induced affective pathology
Gamble-George, J. C., Baldi, R., Halladay, L., Kocharian, A., Hartley, N., Silva, C. G., Roberts, H., Haymer, A., Marnett, L. J., Holmes, A., et al. (2016) · eLife · doi:10.7554/elife.14137 · Cited by 55 · see citing works
TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus
Hurtado-Zavala, J. I., Ramachandran, B., Ahmed, S., Halder, R., Bolleyer, C., Awasthi, A., Stahlberg, M. A., Wagener, R. J., Anderson, K., Drenan, R. M., et al. (2017) · Nature Communications · doi:10.1038/ncomms15878 · Cited by 52 · see citing works
Lee, S.-H., Dudok, B., Parihar, V. K., Jung, K., Zöldi, M., Kang, Y., Maroso, M., Alexander, A., Nelson, G. A., Piomelli, D., et al. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1345-3 · Cited by 53 · see citing works
Self-citationEndocannabinoid Signaling in Motivation, Reward, and Addiction
Sagheddu, C., Muntoni, A. L., Pistis, M., & Melis, M. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.10.004 · Cited by 50 · see citing works
Cannabinoids Modulate Neuronal Activity and Cancer by CB1 and CB2 Receptor-Independent Mechanisms
Soderstrom, K., Soliman, E., & Dross, R. V. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00720 · Cited by 51 · see citing works
Edwards, A., & Abizaid, A. B. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.032 · Cited by 50 · see citing works
Xu, C., Hermes, D. J., Nwanguma, B., Jacobs, I. R., Mackie, K., Mukhopadhyay, S., Lichtman, A. H., Ignatowska-Jankowska, B. M., & Fitting, S. (2017) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2017.07.003 · Cited by 43 · see citing works
Nazıroğlu, M., Taner, A. N., Balbay, E., & Çiğ, B. (2018) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-018-3439-0 · Cited by 43 · see citing works
Colangeli, R., Morena, M., Pittman, Q. J., Hill, M. N., & Teskey, G. C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0068-20.2020 · Cited by 43 · see citing works
Wright, W. J., Schlüter, O. M., & Dong, Y. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.275 · Cited by 35 · see citing works
TRPV1 blockers as potential new treatments for psychiatric disorders
Iglesias, L. P., de Aguiar, D. C., & Moreira, F. A. (2020) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000603 · Cited by 35 · see citing works
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 31 · see citing works
NECAB1 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 29 · see citing works
Self-citationThe role of the cannabinoid system in fear memory and extinction in male and female mice
Mizuno, I., Matsuda, S., Tohyama, S., & Mizutani, A. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105688 · Cited by 35 · see citing works
Hausknecht, K. A., Shen, Y.-L., Wang, R., Haj‐Dahmane, S., & Shen, R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3894-16.2017 · Cited by 32 · see citing works
Manz, K. M., Ghose, D., Turner, B. D., Taylor, A., Becker, J. C., Grueter, C. A., & Grueter, B. A. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107971 · Cited by 33 · see citing works
Multiple cannabinoid signaling cascades powerfully suppress recurrent excitation in the hippocampus
Jensen, K. R., Berthoux, C., Nasrallah, K., & Castillo, P. E. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2017590118 · Cited by 33 · see citing works
Transient Receptor Potential Vanilloid 1 Function at Central Synapses in Health and Disease
Meza, R. C., Ancatén-González, C., Chiu, C. Q., & Chávez, A. E. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.864828 · Cited by 35 · see citing works
Estrada, J. A., & Contreras, I. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200217140255 · Cited by 32 · see citing works
Endocannabinoid-serotonin systems interaction in health and disease
Colangeli, R., Teskey, G. C., & Giovanni, G. D. (2021) · Progress in brain research · doi:10.1016/bs.pbr.2021.01.003 · Cited by 30 · see citing works
Kang, Y., Clement, E. M., Park, I., Greenfield, L. J., Smith, B. N., & Lee, S.-H. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113724 · Cited by 31 · see citing works
Self-citationFowler, C. J., Doherty, P., & Alexander, S. P. H. (2017) · Advances in pharmacology · doi:10.1016/bs.apha.2017.03.006 · Cited by 31 · see citing works
Zádor, F., & Wollemann, M. (2015) · Pharmacological Research · doi:10.1016/j.phrs.2015.10.015 · Cited by 30 · see citing works
Bálint, F., Liposits, Z., & Farkas, I. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00077 · Cited by 30 · see citing works
Sugaya, Y., & Kano, M. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2834-8 · Cited by 29 · see citing works
Zhang, L.-Y., Zhou, Y.-Q., Yu, Z., Zhang, X., Shi, J., & Shen, H. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-00955-1 · Cited by 29 · see citing works
Rapaka, D., Bitra, V. R., Challa, S. R., & Adiukwu, P. C. (2021) · Neuropeptides · doi:10.1016/j.npep.2021.102196 · Cited by 29 · see citing works
Endocannabinoid-Mediated Control of Neural Circuit Excitability and Epileptic Seizures
Sugaya, Y., & Kano, M. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.781113 · Cited by 29 · see citing works
Robinson, S. L., Alexander, N. J., Bluett, R. J., Patel, S., & McCool, B. A. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.12.005 · Cited by 27 · see citing works
Raux, P., Drutel, G., Revest, J., & Vallée, M. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13034 · Cited by 24 · see citing works
Poddighe, L., Carta, G., Serra, M. P., Melis, T., Boi, M., Lisai, S., Murru, E., Muredda, L., Collu, M., Banni, S., et al. (2018) · Lipids in Health and Disease · doi:10.1186/s12944-018-0661-4 · Cited by 25 · see citing works
Pharmacological effects of cannabinoids on learning and memory in Lymnaea
Sunada, H., Watanabe, T., Hatakeyama, D., Lee, S. M., Forest, J., Sakakibara, M., Ito, E., & Lukowiak, K. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.159038 · Cited by 24 · see citing works
Self-citationDong, B., Shilpa, B. M., Shah, R., Goyal, A., Xie, S., Bakalian, M. J., Suckow, R. F., Cooper, T. B., Mann, J. J., Arango, V., et al. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.10.010 · Cited by 24 · see citing works
Chronic Pain and the Endocannabinoid System: Smart Lipids – A Novel Therapeutic Option?
Zieglgänsberger, W., Brenneisen, R., Berthele, A., Wotjak, C. T., Bandelow, B., Tölle, T. R., & Lutz, B. (2022) · Medical Cannabis and Cannabinoids · doi:10.1159/000522432 · Cited by 23 · see citing works
Joffre, J., Wong, E., Lawton, S., Lloyd, E., Nguyen, N. T., Xu, F., Sempio, C., Kobzik, L., Zlatanova, I., Schumacher, M. A., et al. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02485-z · Cited by 23 · see citing works
Xu, C., Hermes, D. J., Mackie, K., Lichtman, A. H., Ignatowska-Jankowska, B. M., & Fitting, S. (2016) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-016-9664-y · Cited by 23 · see citing works
Nawata, Y., Yamaguchi, T., Fukumori, R., & Yamamoto, T. (2018) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyy086 · Cited by 21 · see citing works
Axonal CB1 Receptors Mediate Inhibitory Bouton Formation via cAMP Increase and PKA
Liang, J., Kruijssen, D. L. H., Verschuuren, A. C. J., Voesenek, B. J. B., Benavides, F. F. W., González, M. S., Ruiter, M., & Wierenga, C. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0851-21.2021 · Cited by 20 · see citing works
p21-activated kinase 1 restricts tonic endocannabinoid signaling in the hippocampus
Xia, S., Zhou, Z., Leung, C., Zhu, Y., Pan, X., Qi, J., Morena, M., Hill, M. N., Xie, W., & Jia, Z. (2016) · eLife · doi:10.7554/elife.14653 · Cited by 21 · see citing works
Lazarini-Lopes, W., Silva-Cardoso, G. K., Leite‐Panissi, C. R. A., & Garcia‐Cairasco, N. (2022) · Biomedicines · doi:10.3390/biomedicines10020416 · Cited by 21 · see citing works
Imamura, T., Tsuruma, K., Inoue, Y., Otsuka, T., Ohno, Y., Ogami, S., Yamane, S., Shimazawa, M., & Hara, H. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.03.018 · Cited by 20 · see citing works
Sex differences in endocannabinoid modulation of rat CA1 dendritic neurotransmission
Ferraro, A., Wig, P., Boscarino, J. J., & Reich, C. G. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100283 · Cited by 20 · see citing works
Liput, D. J., Puhl, H. L., Dong, A., He, K., Li, Y., & Lovinger, D. M. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108916 · Cited by 20 · see citing works
Differential Adulthood Onset mGlu5Signaling Saves Prefrontal Function in the Fragile X Mouse
Martin, H. G. S., Lassalle, O., & Manzoni, O. J. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw328 · Cited by 20 · see citing works
Presynaptic nanoscale components of retrograde synaptic signaling
Barti, B., Dudok, B., Kenesei, K., Zöldi, M., Miczán, V., Balla, G. Y., Zala, D., Tasso, M., Sagheddu, C., Kisfali, M., et al. (2024) · Science Advances · doi:10.1126/sciadv.ado0077 · Cited by 19 · see citing works
Self-citationAnstötz, M., Lee, S. K., & Maccaferri, G. (2018) · The Journal of Physiology · doi:10.1113/jp275685 · Cited by 19 · see citing works
Self-citationOubraim, S., Wang, R., Hausknecht, K. A., Shen, R., & Haj‐Dahmane, S. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.691219 · Cited by 18 · see citing works
Noncanonical Activity of Endocannabinoids and Their Receptors in Central and Peripheral Synapses
Balezina, O. P., Tarasova, E. O., & Gaydukov, A. E. (2021) · Biochemistry (Moscow) · doi:10.1134/s0006297921070038 · Cited by 18 · see citing works
Cell Type-specific Intrinsic Perithreshold Oscillations in Hippocampal GABAergic Interneurons
Kang, Y., Lewis, H. E. S., Young, M. W., Govindaiah, G., Greenfield, L. J., García‐Rill, E., & Lee, S.-H. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.02.014 · Cited by 16 · see citing works
Self-citationImaging the endocannabinoid signaling system
Dudok, B., & Soltész, I. (2021) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2021.109451 · Cited by 18 · see citing works
Self-citationQuartu, M., Poddighe, L., Melis, T., Serra, M. P., Boi, M., Lisai, S., Carta, G., Murru, E., Muredda, L., Collu, M., et al. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-016-0389-y · Cited by 17 · see citing works
Ho, H., Fowle, A., Coetzee, M., Greger, I. H., & Watson, J. F. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108824 · Cited by 17 · see citing works
Bálint, F., Csillag, V., Vastagh, C., Liposits, Z., & Farkas, I. (2020) · Neuroendocrinology · doi:10.1159/000514043 · Cited by 17 · see citing works
Petrie, G. N., Balsevich, G., Füzesi, T., Aukema, R. J., Driever, W. P. F., van der Stelt, M., Bains, J. S., & Hill, M. N. (2023) · British Journal of Pharmacology · doi:10.1111/bph.16198 · Cited by 19 · see citing works
Huguet, J. E., Río, I. B., Gómez‐Urquijo, S., Mimenza, A., Saumell-Esnaola, M., Roman, L. B., del Caño, G. G., Sallés, J., Puente, N., Gerrikagoitia, I., et al. (2021) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2021.645940 · Cited by 16 · see citing works
Kang, Y., Lee, S.-H., Boychuk, J. A., Butler, C. R., Juras, J. A., Cloyd, R., & Smith, B. N. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2263-21.2022 · Cited by 15 · see citing works
Self-citationde Souza-Júnior, F. J. C., Cunha, L. C., & Lisboa, S. F. D. S. (2022) · Exploration of Neuroprotective Therapy · doi:10.37349/ent.2022.00028 · Cited by 14 · see citing works
Endocannabinoid interactions in the regulation of acquisition of contextual conditioned fear
Balogh, Z., Szente, L., Bíró, L., Varga, Z. K., Haller, J., & Aliczki, M. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.11.007 · Cited by 14 · see citing works
Xu, C., Yadav-Samudrala, B. J., Xu, C., Nath, B., Mistry, T., Jiang, W., Niphakis, M. J., Cravatt, B. F., Mukhopadhyay, S., Lichtman, A. H., et al. (2022) · Cells · doi:10.3390/cells11050857 · Cited by 13 · see citing works
Iglesias, L. P., Fernandes, H. D. B., de Miranda, A. S., Pérez, M. M., Faccioli, L. H., Sorgi, C. A., Bertoglio, L. J., de Aguiar, D. C., Wotjak, C. T., & Moreira, F. A. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109314 · Cited by 13 · see citing works
Pinheiro, B. S., Lemos, C., Kaufmann, F. N., Marques, J. M., da Silva-Santos, C. S., Carvalho, E., Mackie, K., Rodrigues, R. J., Cunha, R. A., & Köfalvi, A. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.05.009 · Cited by 13 · see citing works
Malhotra, S., Donneger, F., Farrell, J. S., Dudok, B., Losonczy, A., & Soltész, I. (2025) · Neuron · doi:10.1016/j.neuron.2025.03.016 · Cited by 12 · see citing works
Self-citationThe role of the GLP-1/GLP-1R signaling pathway in regulating seizure susceptibility in rats
Zhang, Y., Fang, J., Feng, W., Sun, Q., Xu, J., & Xia, Q. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.06.017 · Cited by 12 · see citing works
Friend, L. N., Williamson, R. C., Merrill, C. B., Newton, S. T., Christensen, M. T., Petersen, J., Wu, B., Ostlund, I., & Edwards, J. G. (2019) · Molecules · doi:10.3390/molecules24071306 · Cited by 12 · see citing works
Koukouli, F., Montmerle, M., Aguirre, A., van Velze, M. D. B., Peixoto, J., Choudhary, V., Varilh, M., Julio‐Kalajzić, F., Allène, C., Méndez, P., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2022.111202 · Cited by 12 · see citing works
Báldi, R., Ghosh, D., Grueter, B. A., & Patel, S. (2016) · Current Protocols in Neuroscience · doi:10.1002/cpns.8 · Cited by 10 · see citing works
The Endocannabinoid System in Prefrontal Synaptopathies
Scheyer, A. F., Martin, H. G. S., & Manzoni, O. J. (2017) · Springer eBooks · doi:10.1007/978-3-319-57371-7_7 · Cited by 10 · see citing works
Circuit mechanisms governing endocannabinoid modulation of affective behaviour and stress adaptation
Loomba, N., & Patel, S. (2025) · Nature reviews. Neuroscience · doi:10.1038/s41583-025-00961-y · Cited by 10 · see citing works
Jamieson, B. B., Kim, J. S., & Iremonger, K. J. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13084 · Cited by 9 · see citing works
Cristino, L., Imperatore, R., & Marzo, V. D. (2017) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2017.05.003 · Cited by 9 · see citing works
SGIP1 in axons prevents internalization of desensitized CB1R and modifies its function
Durydivka, O., Mackie, K., & Blahoš, J. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1213094 · Cited by 8 · see citing works
Loren Parsons' contribution to addiction neurobiology
Luca, M. A. D., Buczynski, M. W., & Chiara, G. D. (2018) · Addiction Biology · doi:10.1111/adb.12642 · Cited by 8 · see citing works
Guo, Z., Tse, Y. C., Zhang, Y., Sun, Q., Vecchiarelli, H. A., Aukema, R. J., Hill, M. N., Wong, T. P., & Boksa, P. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.09.003 · Cited by 8 · see citing works
Endocannabinoids regulate cocaine-associated memory through brain AEA–CB1R signalling activation
Li, H., Chen, R., Zhou, Y., Wang, H., Sun, L., Yang, Z., Bai, L., & Zhang, J. (2022) · Molecular Metabolism · doi:10.1016/j.molmet.2022.101597 · Cited by 8 · see citing works
Soni, N., Prabhala, B. K., Mehta, V., Mirza, O., & Kohlmeier, K. A. (2017) · Brain Research · doi:10.1016/j.brainres.2017.04.003 · Cited by 8 · see citing works
- Authors
- Lee, S.-H., Ledri, M., Toth, B., Marchionni, I., Henstridge, C. M., Dudok, B., Kenesei, K., Barna, L., Szabo, S. I., Renkecz, T., Oberoi, M., Watanabe, M., Limoli, C. L., Horvai, G., Soltesz, I., & Katona, I.
- Affiliations
- University of California, Irvine (US)
- HUN-REN Institute of Experimental Medicine (HU)
- Semmelweis University (HU)
- Budapest University of Technology and Economics (HU)
- Hokkaido University (JP)
- ORCID
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-07-08
- Volume
- 35
- Issue
- 27
- Pages
- 10039-10057
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4495235
- OpenAlex
- W1892287994
- Cited by
- 133
- References
- 115
- Citations by year
- 2026: 1 · 2025: 10 · 2024: 6 · 2023: 6 · 2022: 18 · 2021: 18 · 2020: 8 · 2019: 4 · 2018: 13 · 2017: 23 · 2016: 19 · 2015: 6
- FWCI
- 14.65
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Padua Research Archive (University of Padova) (submittedVersion, other-oa)
- Discovery Research Portal (University of Dundee) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Padua Research Archive (University of Padova) (submittedVersion)
- Funders
- National Aeronautics and Space Administration (NNX10AD59G, NNX15AI22G)
- Wellcome Trust (090946)
- Magyar Tudományos Akadémia
- National Institutes of Health (CA-62203, NS35915)
- University of California, Irvine (CA-62203)
- National Cancer Institute (CA 62203, P30CA062203)
- National Institute of General Medical Sciences (GM-69337, T34GM069337)
- National Institute of Neurological Disorders and Stroke (R29NS035915, R01NS035915, NS-35915, R37NS035915)
- FP7 Ideas: European Research Council (243153)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Keywords
- endocannabinoid signaling, CB1 receptor, tonic inhibition, GABA release, 2-arachidonoylglycerol, anandamide, monoacylglycerol lipase, fatty acid amide hydrolase, TRPV1, presynaptic inhibition, hippocampus, CA1 pyramidal neurons
- MeSH terms
- Animals, Arachidonic Acids, Enzyme Inhibitors, Female, gamma-Aminobutyric Acid, Glycerides, Hippocampus, Male, Mice, Inbred C57BL, Mice, Transgenic, Neurons, Piperidines, Pyrazoles, Pyridines, Synapses, Signal Transduction, Receptor, Cannabinoid, CB1, TRPV Cation Channels, Mice, Inhibitory Postsynaptic Potentials, Cannabinoid Receptor Modulators, Endocannabinoids
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 ›
Are you an author, or do you see a problem with this page? Request a review
