Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-27T08:56:39.072Z Has data issue: false hasContentIssue false

Interplay between endocannabinoid and endovanilloid mechanisms in fear conditioning

Published online by Cambridge University Press:  20 November 2023

Rayssa C. Briânis
Affiliation:
Department of Pharmacology, Institute of Biological Sciences; Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Julia P. Andreotti
Affiliation:
Department of Pharmacology, Institute of Biological Sciences; Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Fabrício A. Moreira
Affiliation:
Department of Pharmacology, Institute of Biological Sciences; Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
Lia P. Iglesias*
Affiliation:
Department of Pharmacology, Institute of Biological Sciences; Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
*
Corresponding author: L. P. Iglesias; Email: liaparadaiglesias@gmail.com

Abstract

Objective:

The transient receptor potential cation channel, subfamily V (vanilloid), member 1 (TRPV1) mediates pain perception to thermal and chemical stimuli in peripheral neurons. The cannabinoid receptor type 1 (CB1), on the other hand, promotes analgesia in both the periphery and the brain. TRPV1 and CB1 have also been implicated in learned fear, which involves the association of a previously neutral stimulus with an aversive event. In this review, we elaborate on the interplay between CB1 receptors and TRPV1 channels in learned fear processing.

Methods:

We conducted a PubMed search for a narrative review on endocannabinoid and endovanilloid mechanisms on fear conditioning.

Results:

TRPV1 and CB1 receptors are activated by a common endogenous agonist, arachidonoyl ethanolamide (anandamide), Moreover, they are expressed in common neuroanatomical structures and recruit converging cellular pathways, acting in concert to modulate fear learning. However, evidence suggests that TRPV1 exerts a facilitatory role, whereas CB1 restrains fear responses.

Conclusion:

TRPV1 and CB1 seem to mediate protective and aversive roles of anandamide, respectively. However, more research is needed to achieve a better understanding of how these receptors interact to modulate fear learning.

Type
Review Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of Scandinavian College of Neuropsychopharmacology

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abush, H and Akirav, I (2010) Cannabinoids modulate hippocampal memory and plasticity. Hippocampus 20(10), 11261138.CrossRefGoogle ScholarPubMed
Alexandra Kredlow, M, Fenster, RJ, Laurent, ES, Ressler, KJ, Phelps, EA (2022) Prefrontal cortex, amygdala, and threat processing: implications for PTSD. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology 47(1), 247259.CrossRefGoogle ScholarPubMed
Alger, BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Progress in Neurobiology 68(4), 247286.CrossRefGoogle ScholarPubMed
Almeida, V, Levin, R, Peres, FF, Suiama, MA, Vendramini, AM, Santos, CM, Silva, ND, Zuardi, AW, Hallak, JEC, Crippa, JA and Abílio, VC (2019) Role of the endocannabinoid and endovanilloid systems in an animal model of schizophrenia-related emotional processing/cognitive deficit. Neuropharmacology 155, 4453.CrossRefGoogle Scholar
Asok, A, Leroy, F, Rayman, JB and Kandel, ER (2019) Molecular mechanisms of the memory trace. Trends in Neurosciences 42(1), 1422.CrossRefGoogle ScholarPubMed
Auber, A, Tedesco, V, Jones, CE, Monfils, M-H and Chiamulera, C (2013) Post-retrieval extinction as reconsolidation interference: methodological issues or boundary conditions? Psychopharmacology 226(4), 631647.CrossRefGoogle ScholarPubMed
Bacci, A, Huguenard, JR, Prince, DA (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431(7006), 312316.CrossRefGoogle ScholarPubMed
Back, FP and Carobrez, AP (2018) Periaqueductal gray glutamatergic, cannabinoid and vanilloid receptor interplay in defensive behavior and aversive memory formation. Neuropharmacology 135, 399411.CrossRefGoogle ScholarPubMed
Balogh, Z, Szente, L, Biro, L, Varga, ZK, Haller, J and Aliczki, M (2019) Endocannabinoid interactions in the regulation of acquisition of contextual conditioned fear. Progress in Neuro-psychopharmacology & Biological Psychiatry 90(84-91), 8491.CrossRefGoogle ScholarPubMed
Basavarajappa, BS, Nagre, NN, Xie, S and Subbanna, S (2014) Elevation of endogenous anandamide impairs LTP, learning, and memory through CB1 receptor signaling in mice. Hippocampus 24(7), 808818.CrossRefGoogle ScholarPubMed
Bienvenu, TCM, Dejean, C, Jercog, D, Aouizerate, B, Lemoine, M and Herry, C (2021) The advent of fear conditioning as an animal model of post-traumatic stress disorder: learning from the past to shape the future of PTSD research. Neuron 109(15), 23802397.CrossRefGoogle ScholarPubMed
Bitencourt, RM, Pamplona, FA and Takahashi, RN (2008) Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. European Neuropsychopharmacology 18(12), 849859.CrossRefGoogle ScholarPubMed
Blázquez, C, Chiarlone, A, Bellocchio, L, Resel, E, Pruunsild, P, García-Rincón, D, Sendtner, M, Timmusk, T, Lutz, B, Galve-Roperh, I and Guzmán, M (2015) The CB1 cannabinoid receptor signals striatal neuroprotection via a PI3K/Akt/mTORC1/BDNF pathway. Cell Death and Differentiation 22(10), 16181629.CrossRefGoogle Scholar
Brianis, RC, Lima, RC, Moreira, FA and Aguiar, DC (2022) Anti-aversive effect of 2-arachidonoylglycerol in the dorsolateral periaqueductal gray of male rats in contextual fear conditioning and Vogel tests. Behavioural Pharmacology 33(2&3), 213221.CrossRefGoogle ScholarPubMed
Burman, MA, Szolusha, K, Bind, R, Kerney, K, Boger, DL and Bilsky, EJ (2016) FAAH inhibitor OL-135 disrupts contextual, but not auditory, fear conditioning in rats. Behavioural Brain Research 308, 15.CrossRefGoogle Scholar
Busquets-Garcia, A, Bains, J and Marsicano, G (2018) CB receptor signaling in the brain: extracting specificity from ubiquity. Neuropsychopharmacology 43(1), 420.CrossRefGoogle ScholarPubMed
Casarotto, PC, Terzian, ALB, Aguiar, DC, Zangrossi, H, Guimarães, FS, Wotjak, CT and Moreira, FA (2012) Opposing roles for cannabinoid receptor type-1 (CB1) and transient receptor potential vanilloid type-1 channel (TRPV1) on the modulation of panic-like responses in rats. Neuropsychopharmacology 37(2), 478486.CrossRefGoogle ScholarPubMed
Caterina, MJ, Schumacher, MA, Tominaga, M, Rosen, TA, Levine, JD and Julius, D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389(6653), 816824.CrossRefGoogle ScholarPubMed
Cavener, VS, Gaulden, A, Pennipede, D, Jagasia, P, Uddin, J, Marnett, LJ and Patel, S (2018) Inhibition of diacylglycerol lipase impairs fear extinction in mice. Frontiers in Neuroscience 12, 479.CrossRefGoogle ScholarPubMed
Conoscenti, MA and Fanselow, MS (2019) Dissociation in effective treatment and behavioral phenotype between stress-enhanced fear learning and learned helplessness. Frontiers in Behavioral Neuroscience 13, 104.CrossRefGoogle ScholarPubMed
Cristino, L, de Petrocellis, L, Pryce, G, Baker, D, Guglielmotti, V and Di Marzo, V (2006) Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139(4), 14051415.CrossRefGoogle ScholarPubMed
Cristino, L, Bisogno, T and Di Marzo, V (2020) Cannabinoids and the expanded endocannabinoid system in neurological disorders. Nature Reviews Neurology 16(1), 929.CrossRefGoogle ScholarPubMed
Cui, Y, Paillé, V, Xu, H, Genet, S, Delord, B, Fino, E, Berry, H and Venance, L (2015) Endocannabinoids mediate bidirectional striatal spike-timing-dependent plasticity. The Journal of Physiology 593(13), 28332849.CrossRefGoogle ScholarPubMed
Cui, Y, Perez, S and Venance, L (2018) Endocannabinoid-LTP mediated by CB1 and TRPV1 receptors encodes for limited occurrences of coincident activity in neocortex. Frontiers in Cellular Neuroscience 12, 182.CrossRefGoogle ScholarPubMed
De Petrocellis, L, Harrison, S, Bisogno, T, Tognetto, M, Brandi, I, Smith, GD, Creminon, C, Davis, JB, Geppetti, P and Di Marzo, V (2001) The vanilloid receptor (VR1)-mediated effects of anandamide are potently enhanced by the cAMP-dependent protein kinase. Journal of Neurochemistry 77(6), 16601663.CrossRefGoogle ScholarPubMed
Deutsch, DG and Chin, SA (1993) Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochemical Pharmacology 46(5), 791796.CrossRefGoogle ScholarPubMed
Devane, WA, Dysarz, FA, Johnson, MR, Melvin, LS and Howlett, AC (1988) Determination and characterization of a cannabinoid receptor in rat brain. Molecular Pharmacology 34(5), 605613.Google ScholarPubMed
Devane, WA, Hanuš, L, Breuer, A, Pertwee, RG, Stevenson, LA, Griffin, G, Gibson, D, Mandelbaum, A, Etinger, A and Mechoulam, R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258(5090), 19461949.CrossRefGoogle Scholar
Dinh, TP, Carpenter, D, Leslie, FM, Freund, TF, Katona, I, Sensi, SL, Kathuria, S and Piomelli, D (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proceedings of The National Academy of Sciences of The United States of America 99(16), 1081910824.CrossRefGoogle ScholarPubMed
Diniz, CRAF, Biojone, C, Joca, SRL, Rantamäki, T, Castrén, E, Guimarães, FS and Casarotto, PC (2019) Dual mechanism of TRKB activation by anandamide through CB1 and TRPV1 receptors. Peer Journal 7, e6493.CrossRefGoogle ScholarPubMed
Docherty, RJ, Yeats, JC, Bevan, S and Boddeke, HW (1996) Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflugers Archiv: European Journal of Physiology 431(6), 828837.CrossRefGoogle ScholarPubMed
Dos Anjos-Garcia, T and Coimbra, NC (2019) Opposing roles of dorsomedial hypothalamic CB1 and TRPV1 receptors in anandamide signaling during the panic-like response elicited in mice by Brazilian rainbow boidae snakes. Psychopharmacology 236(6), 18631874.CrossRefGoogle ScholarPubMed
Fanselow, MS and Pennington, ZT (2018) A return to the psychiatric dark ages with a two-system framework for fear. Behaviour Research and Therapy 100, 2429.CrossRefGoogle Scholar
Foa, EB, Steketee, G and Rothbaum, BO (1989) Behavioral/cognitive conceptualizations of post-traumatic stress disorder. Behavior Therapy 20(ue 2), 155176.CrossRefGoogle Scholar
Fogaça, MV, Aguiar, DC, Moreira, FA and Guimarães, FS (2012) The endocannabinoid and endovanilloid systems interact in the rat prelimbic medial prefrontal cortex to control anxiety-like behavior. Neuropharmacology 63(2), 202210.CrossRefGoogle ScholarPubMed
Gaspar, JC, Okine, BN, Dinneen, D, Roche, M and Finn, DP (2022) Effects of intra-BLA administration of PPAR antagonists on Formalin-evoked nociceptive behaviour, fear-conditioned analgesia, and conditioned fear in the presence or absence of nociceptive tone in rats. Molecules 27(6), 2021.CrossRefGoogle ScholarPubMed
Genro, BP, de Oliveira, AL and Quillfeldt, JA (2012) Role of TRPV1 in consolidation of fear memories depends on the averseness of the conditioning procedure. Neurobiology of Learning and Memory 97(4), 355360.CrossRefGoogle ScholarPubMed
Gobira, PH, Lima, IV, Batista, LA de Oliveira, AC, Resstel, LB, Wotjak, CT, Aguiar, DC, Moreira, FA (2017) N-arachidonoyl-serotonin, a dual FAAH and TRPV1 blocker, inhibits the retrieval of contextual fear memory: role of the cannabinoid CB1 receptor in the dorsal hippocampus. Journal of Psychopharmacology 31(6), 750756.CrossRefGoogle ScholarPubMed
Gomes-de-Souza, L, Bianchi, PC, Costa-Ferreira, W, Tomeo, RA, Cruz, FC and Crestani, CC (2021) CB and CB receptors in the bed nucleus of the stria terminalis differently modulate anxiety-like behaviors in rats. Progress in Neuro-psychopharmacology & Biological Psychiatry 110, 110284.CrossRefGoogle ScholarPubMed
Grueter, BA, Brasnjo, G and Malenka, RC (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nature Neuroscience 13(12), 15191525.CrossRefGoogle ScholarPubMed
Gulyas, AI, Cravatt, BF, Bracey, MH, Dinh, TP, Piomelli, D, Boscia, F and Freund, TF (2004) Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. The European Journal of Neuroscience 20(2), 441458.CrossRefGoogle ScholarPubMed
Hennings, AC, Cooper, SE, Lewis-Peacock, JA and Dunsmoor, JE (2022) Pattern analysis of neuroimaging data reveals novel insights on threat learning and extinction in humans. Neuroscience and Biobehavioral Reviews 142, 104918.CrossRefGoogle ScholarPubMed
Howlett, AC, Barth, F, Bonner, TI, Cabral, G, Casellas, P, Devane, WA, Felder, CC, Herkenham, M, Mackie, K, Martin, BR, Mechoulam, R and Pertwee, RG (2002) International union of pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacological Reviews 54(2), 161202.Google ScholarPubMed
Huang, EP (1997) Synaptic plasticity: a role for nitric oxide in LTP. Current Biology: CB 7(3), R1413.CrossRefGoogle ScholarPubMed
Huang, WX, Min, JW, Liu, YQ, He, XH and Peng, BW (2014) Expression of TRPV1 in the C57BL/6 mice brain hippocampus and cortex during development. Neuroreport 25(6), 379385.CrossRefGoogle ScholarPubMed
Hurtado-Zavala, JI, Ramachandran, B, Ahmed, S, Halder, R, Bolleyer, C, Awasthi, A, Stahlberg, MA, Wagener, RJ, Anderson, K, Drenan, RM, Lester, HA, Miwa, JM, Staiger, JF, Fischer, A and Dean, C (2017) TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus. Nature Communications 8(1), 15878.CrossRefGoogle ScholarPubMed
Iglesias, LP, Fernandes, HB, de Miranda, AS, Perez, MM, Faccioli, LH, Sorgi, CA, Bertoglio, LJ, Aguiar, DC, Wotjak, CT and Moreira, FA (2023) TRPV1 modulation of contextual fear memory depends on stimulus intensity and endocannabinoid signalling in the dorsal hippocampus. Neuropharmacology 224, 109314.CrossRefGoogle ScholarPubMed
Jamieson, BB, Kim, JS and Iremonger, KJ (2022) Cannabinoid and vanilloid pathways mediate opposing forms of synaptic plasticity in corticotropin-releasing hormone neurons. Journal of Neuroendocrinology 34(4), e13084.CrossRefGoogle ScholarPubMed
Josselyn, SA, Köhler, S and Frankland, PW (2015) Finding the engram. Nature Reviews. Neuroscience 16(9), 521534.CrossRefGoogle ScholarPubMed
Josselyn, SA and Tonegawa, S (2020) Memory engrams: recalling the past and imagining the future. Science 367(6473).CrossRefGoogle ScholarPubMed
Katona, I, Sperlágh, B, Sík, A, Käfalvi, A, Vizi, ES, Mackie, K and Freund, TF (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. The Journal of Neuroscience 19(11), 45444558.CrossRefGoogle ScholarPubMed
Krause, MA and Domjan, M (2017) Ethological and evolutionary perspectives on pavlovian conditioning, in APA handbook of comparative psychology: perception, learning, and cognition . Washington: American Psychological Association, 247266.CrossRefGoogle Scholar
Lagatta, DC, Kuntze, LB, Ferreira-Junior, NC and Resstel, LBM (2018) Medial prefrontal cortex TRPV1 and CB1 receptors modulate cardiac baroreflex activity by regulating the NMDA receptor/nitric oxide pathway. Pflugers Archiv: European Journal of Physiology 470(10), 15211542.CrossRefGoogle ScholarPubMed
Laricchiuta, D, Centonze, D and Petrosini, L (2013) Effects of endocannabinoid and endovanilloid systems on aversive memory extinction. Behavioural Brain Research 256, 101107.CrossRefGoogle ScholarPubMed
Lazenka, MF, Selley, DE, Sim-Selley, LJ (2013) Brain regional differences in CB1 receptor adaptation and regulation of transcription. Life Sciences 92(8-9), 446452.CrossRefGoogle ScholarPubMed
Lee, H and Kaang, B-K (2023) How engram mediates learning, extinction, and relapse. Current Opinion in Neurobiology 81, 102723.CrossRefGoogle ScholarPubMed
Liu, P, Bilkey, DK, Darlington, CL and Smith, PF (2003) Cannabinoid CB1 receptor protein expression in the rat hippocampus and entorhinal, perirhinal, postrhinal and temporal cortices: regional variations and age-related changes. Brain Research 979(1-2), 235239.CrossRefGoogle ScholarPubMed
Lin, Q-S, Yang, Q, Liu, D-D, Sun, Z, Dang, H, Liang, J, Wang, YX, Chen, J and Li, S-T (2011) Hippocampal endocannabinoids play an important role in induction of long-term potentiation and regulation of contextual fear memory formation. Brain Research Bulletin 86(3-4), 139145.CrossRefGoogle ScholarPubMed
Lisboa, SF, Reis, DG, da Silva, AL, Corrêa, FMA, Guimarães, FS and Resstel, LBM (2010) Cannabinoid CB1 receptors in the medial prefrontal cortex modulate the expression of contextual fear conditioning. The international Journal of Neuropsychopharmacology 13(9), 11631173.CrossRefGoogle ScholarPubMed
Lisboa, SF, Gomes, FV, Silva, AL, Uliana, DL, Camargo, LHA, Guimarães, FS, Cunha, FQ, Joca, SRL and Resstel, LBM (2015) Increased contextual fear conditioning in iNOS knockout mice: additional evidence for the involvement of nitric oxide in stress-related disorders and contribution of the endocannabinoid system. The International Journal of Neuropsychopharmacology 18(8), pyv005pyv005.CrossRefGoogle ScholarPubMed
Lishko, PV, Procko, E, Jin, X, Phelps, CB and Gaudet, R (2007) The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54(6), 905918.CrossRefGoogle ScholarPubMed
Li, Y, Zhi, W, Qi, B, Wang, L and Hu, X (2023) Update on neurobiological mechanisms of fear: illuminating the direction of mechanism exploration and treatment development of trauma and fear-related disorders. Frontiers in Behavioral Neuroscience 17, 1216524.CrossRefGoogle ScholarPubMed
Llorente-Berzal, A, Terzian, ALB, di Marzo, V, Micale, V, Viveros, MP and Wotjak, CT (2015) 2-AG promotes the expression of conditioned fear via cannabinoid receptor type 1 on GABAergic neurons. Psychopharmacology 232(15), 28112825.CrossRefGoogle ScholarPubMed
Lutz, B, Marsicano, G, Maldonado, R and Hillard, CJ (2015) The endocannabinoid system in guarding against fear, anxiety and stress. Nature Reviews. Neuroscience 16(12), 705718.CrossRefGoogle ScholarPubMed
Luyten, L, Vansteenwegen, D, van Kuyck, K, Gabriëls, L and Nuttin, B (2011) Contextual conditioning in rats as an animal model for generalized anxiety disorder. Cognitive, Affective & Behavioral Neuroscience 11(2), 228244.CrossRefGoogle ScholarPubMed
Maccarrone, M, Rossi, S, Bari, M, De Chiara, V, Fezza, F, Musella, A, Gasperi, V, Prosperetti, C, Bernardi, G, Finazzi-Agrò, A, Cravatt, BF and Centonze, D (2008) Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum. Nature Neuroscience 11(2), 152159.CrossRefGoogle ScholarPubMed
Maćkowiak, M, Chocyk, A, Dudys, D and Wedzony, K (2009) Activation of CB1 cannabinoid receptors impairs memory consolidation and hippocampal polysialylated neural cell adhesion molecule expression in contextual fear conditioning. Neuroscience 158(4), 17081716.CrossRefGoogle ScholarPubMed
Marinelli, S, Pascucci, T, Bernardi, G, Puglisi-Allegra, S and Mercuri, NB (2005) Activation of TRPV1 in the VTA excites dopaminergic neurons and increases chemical- and noxious-induced dopamine release in the nucleus accumbens. Neuropsychopharmacology 30(5), 864870.CrossRefGoogle ScholarPubMed
Marks, WD, Yokose, J, Kitamura, T and Ogawa, SK (2022) Neuronal ensembles organize activity to generate contextual memory. Frontiers in Behavioral Neuroscience 16, 805132.CrossRefGoogle ScholarPubMed
Maroso, M, Szabo, GG, Kim, HK, Alexander, A, Bui, AD, Lee, SH, Lutz, B and Soltesz, I (2016) Cannabinoid control of learning and memory through HCN channels. Neuron 89(5), 10591073.CrossRefGoogle ScholarPubMed
Marsch, R, Foeller, E, Rammes, G, Bunck, M, Kössl, M, Holsboer, F, Zieglgänsberger, W, Landgraf, R, Lutz, B and Wotjak, CT (2007) Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. The Journal of Neuroscience 27(4), 832839.CrossRefGoogle ScholarPubMed
Marsicano, G, Wotjak, CT, Azad, SC, Bisogno, T, Rammes, G, Cascio, MG, Hermann, H, Tang, J, Hofmann, C, Zieglgänsberger, W, Di Marzo, V and Lutz, B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418(6897), 530534.CrossRefGoogle ScholarPubMed
Matsuda, LA, Lolait, SJ, Brownstein, MJ, Young, AC and Bonner, TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346(6284), 561564.CrossRefGoogle ScholarPubMed
Mechoulam, R, Ben-Shabat, S, Hanus, L, Ligumsky, M, Kaminski, NE, Schatz, AR, Gopher, A, Almog, S, Martin, BR, Compton, DR, Pertwee, RG, Griffin, G, Bayewitch, M, Barg, J, Vogel, Z (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochemical Pharmacology 50(1), 8390.CrossRefGoogle ScholarPubMed
Medeiros, KAAL, Almeida-Souza, TH, Silva, RS, Santos, HF, Santos, EV, Gois, AM, Leal, PC and Santos, JR (2022) Involvement of nitric oxide in the neurobiology of fear-like behavior. Nitric Oxide 124, 2431.CrossRefGoogle ScholarPubMed
Milton, AL (2019) Fear not: recent advances in understanding the neural basis of fear memories and implications for treatment development . F1000Research 8.Google Scholar
Minichiello, L (2009) TrkB signalling pathways in LTP and learning. Nature Reviews. Neuroscience 10(12), 850860.CrossRefGoogle ScholarPubMed
Mizuno, I, Matsuda, S, Tohyama, S and Mizutani, A (2022) The role of the cannabinoid system in fear memory and extinction in male and female mice. Psychoneuroendocrinology 138, 105688.CrossRefGoogle ScholarPubMed
Morena, M, Roozendaal, B, Trezza, V, Ratano, P, Peloso, A, Hauer, D, Atsak, P, Trabace, L, Cuomo, V, McGaugh, JL, Schelling, G and Campolongo, P (2014) Endogenous cannabinoid release within prefrontal-limbic pathways affects memory consolidation of emotional training. Proceedings of the National Academy of Sciences of the United States of America 111(51), 1833318338.CrossRefGoogle ScholarPubMed
Morena, M, Nastase, AS, Santori, A, Cravatt, BF, Shansky, RM and Hill, MN (2021) Sex-dependent effects of endocannabinoid modulation of conditioned fear extinction in rats. British Journal of Pharmacology 178(4), 983996. https://doi.org/10.1111/bph.15341.CrossRefGoogle ScholarPubMed
Munro, S, Thomas, KL and Abu-Shaar, M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365(6441), 6165.CrossRefGoogle ScholarPubMed
Naidu, PS, Varvel, SA, Ahn, K, Cravatt, BF, Martin, BR and Lichtman, AH (2007) Evaluation of fatty acid amide hydrolase inhibition in murine models of emotionality. Psychopharmacology 192(1), 6170.CrossRefGoogle ScholarPubMed
Nasehi, M, Davoudi, K, Ebrahimi-Ghiri, M and Zarrindast, M-R (2016) Interplay between serotonin and cannabinoid function in the amygdala in fear conditioning. Brain Research 142, 1636–1151.Google Scholar
Navabpour, S, Rezayof, A and Ghasemzadeh, Z (2021) Activation of VTA/CeA/mPFC cannabinoid CB1 receptors induced conditioned drug effects via interacting with hippocampal CAMKII-CREB-BDNF signaling pathway in rats. European Journal of Pharmacology 909, 174417.CrossRefGoogle ScholarPubMed
Notaras, M and van den Buuse, M (2020) Neurobiology of BDNF in fear memory, sensitivity to stress, and stress-related disorders. Molecular Psychiatry 25(10), 22512274.CrossRefGoogle ScholarPubMed
Numazaki, M, Tominaga, T, Takeuchi, K, Murayama, N, Toyooka, H and Tominaga, M (2003) Structural determinant of TRPV1 desensitization interacts with calmodulin. Proceedings of the National Academy of Sciences of the United States of America 100(13), 80028006.CrossRefGoogle ScholarPubMed
Ohno-Shosaku, T, Maejima, T and Kano, M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29(3), 729738.CrossRefGoogle ScholarPubMed
de Oliveira, AL, Pasqualini, GB, Diehl, F, Molina, VA and Quillfeldt, JA (2008) Opposite action of hippocampal CB1 receptors in memory reconsolidation and extinction. Neuroscience 154(4), 16481655.CrossRefGoogle Scholar
de Oliveira, AL and Do-Monte, FH (2021) Understanding the dynamic and destiny of memories. Neuroscience and Biobehavioral Reviews 125, 592607.CrossRefGoogle Scholar
Pamplona, FA, Prediger, RDS, Pandolfo, P and Takahashi, RN (2006) The cannabinoid receptor agonist WIN 55,212-2 facilitates the extinction of contextual fear memory and spatial memory in rats. Psychopharmacology 188(4), 641649.CrossRefGoogle ScholarPubMed
Pamplona, FA and Takahashi, RN (2006) WIN 55212-2 impairs contextual fear conditioning through the activation of CB1 cannabinoid receptors. Neuroscience Letters 397(1-2), 8892.CrossRefGoogle ScholarPubMed
Pamplona, FA, Bitencourt, RM and Takahashi, RN (2008) Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats. Neurobiology of Learning and Memory 90(1), 290293.CrossRefGoogle Scholar
Pedroza-Llinás, R, Méndez-Díaz, M, Ruiz-Contreras, AE and Prospéro-García, Ó. (2013) CB1 receptor activation in the nucleus accumbens core impairs contextual fear learning. Behavioural Brain Research 237, 141147.CrossRefGoogle ScholarPubMed
Phillips, RG and LeDoux, JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 106(2), 274285.CrossRefGoogle ScholarPubMed
Piomelli, D, Mabou Tagne, A (2022) Endocannabinoid-based therapies. Annual Review of Pharmacology and Toxicology 62(1), 483507.CrossRefGoogle ScholarPubMed
Premkumar, LS and Ahern, GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408(6815), 985990.CrossRefGoogle ScholarPubMed
Ray, MH, Russ, AN, Walker, RA and McDannald, MA (2020) The nucleus accumbens core is necessary to scale fear to degree of threat. The Journal of Neuroscience 40(24), 47504760.CrossRefGoogle ScholarPubMed
Reich, CG, Mohammadi, MH and Alger, BE (2008) Endocannabinoid modulation of fear responses: learning and state-dependent performance effects. Journal of Psychopharmacology 22(7), 769777.CrossRefGoogle ScholarPubMed
Resstel, LBM, Lisboa, SF, Aguiar, DC, Corrêa, FMA and Guimarães, FS (2008) Activation of CB1 cannabinoid receptors in the dorsolateral periaqueductal gray reduces the expression of contextual fear conditioning in rats. Psychopharmacology 198(3), 405411.CrossRefGoogle ScholarPubMed
Ross, RA (2003) Anandamide and vanilloid TRPV1 receptors. British Journal of Pharmacology 140(5), 790801.CrossRefGoogle ScholarPubMed
Sadeghi, MA, Hemmati, S, Nassireslami, E, Yousefi, ZM, Hosseini, Y, Abbasian, K and Chamanara, M (2022) Targeting neuronal nitric oxide synthase and the nitrergic system in post-traumatic stress disorder. Psychopharmacology 239(10), 30573082.CrossRefGoogle ScholarPubMed
Scienza-Martin, K, Lotz, FN, Zanona, QK, Santana-Kragelund, F, Crestani, AP, Boos, FZ, Calcagnotto, ME and Quillfeldt, JA (2022) Memory consolidation depends on endogenous hippocampal levels of anandamide: CB1 and M4, but possibly not TRPV1 receptors mediate AM404 effects. Neuroscience 497, 5372.CrossRefGoogle Scholar
Simone, JJ, Green, MR, Hodges, TE and McCormick, CM (2015) Differential effects of CB1 receptor agonism in behavioural tests of unconditioned and conditioned fear in adult male rats. Behavioural Brain Research 279, 916.CrossRefGoogle ScholarPubMed
Sink, KS, Segovia, KN, Collins, LE, Markus, EJ, Vemuri, VK, Makriyannis, A and Salamone, JD (2010) The CB1 inverse agonist AM251, but not the CB1 antagonist AM4113, enhances retention of contextual fear conditioning in rats. Pharmacology, Biochemistry, and Behavior 95(4), 479484.CrossRefGoogle Scholar
Starowicz, K, Maione, S, Cristino, L, Palazzo, E, Marabese, I, Rossi, F, de Novellis, V and Di Marzo, V (2007) Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. The Journal of Neuroscience 27(50), 1373913749.CrossRefGoogle ScholarPubMed
van der Stelt, M, Trevisani, M, Vellani, V, De Petrocellis, L, Schiano Moriello, A, Campi, B, McNaughton, P, Geppetti, P and Di Marzo, V (2005) Anandamide acts as an intracellular messenger amplifying Ca2 influx via TRPV1 channels. The EMBO Journal 24(19), 35173518.CrossRefGoogle ScholarPubMed
Stern, CAJ, da Silva, TR, Raymundi, AM, de Souza, CP, Hiroaki-Sato, VA, Kato, L, Guimarães, FS, Andreatini, R, Takahashi, RN and Bertoglio, LJ (2017) Cannabidiol disrupts the consolidation of specific and generalized fear memories via dorsal hippocampus CB1 and CB2 receptors. Neuropharmacology 125, 220230.CrossRefGoogle Scholar
Susswein, AJ, Katzoff, A, Miller, N and Hurwitz, I (2004) Nitric oxide and memory. The Neuroscientist 10(2), 153162.CrossRefGoogle ScholarPubMed
Szallasi, A and Di Marzo, V (2000) New perspectives on enigmatic vanilloid receptors. Trends in Neurosciences 23(10), 491497.CrossRefGoogle ScholarPubMed
Tahmasebi, L, Komaki, A, Karamian, R, Shahidi, S, Sarihi, A, Salehi, I and Nikkhah, A (2015) The interactive role of cannabinoid and vanilloid systems in hippocampal synaptic plasticity in rats. European Journal of Pharmacology 757, 6873.CrossRefGoogle ScholarPubMed
Terzian, ALB, dos Reis, DG, Guimarães, FS, Corrêa, FMA and Resstel, LBM (2014) Medial prefrontal cortex transient receptor potential vanilloid type 1 (TRPV1) in the expression of contextual fear conditioning in Wistar rats. Psychopharmacology 231(1), 149157.CrossRefGoogle ScholarPubMed
Thomas, KL, Hall, J and Everitt, BJ (2002) Cellular imaging with zif268 expression in the rat nucleus accumbens and frontal cortex further dissociates the neural pathways activated following the retrieval of contextual and cued fear memory. The European Journal of Neuroscience 16(9), 17891796.CrossRefGoogle ScholarPubMed
Tóth, A, Boczán, J, Kedei, N, Lizanecz, E, Bagi, Z, Papp, Z, Edes, I, Csiba, L and Blumberg, PM (2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Research 135(1-2), 162168.Google ScholarPubMed
Tsou, K, Brown, S, Sañudo-Peña, MC, Mackie, K and Walker, JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83(2), 393411.CrossRefGoogle ScholarPubMed
Uchigashima, M, Narushima, M, Fukaya, M, Katona, I, Kano, M and Watanabe, M (2007) Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. The Journal of Neuroscience 27(14), 36633676.CrossRefGoogle ScholarPubMed
Uliana, DL, Hott, SC, Lisboa, SF and Resstel, LBM (2016) Dorsolateral periaqueductal gray matter CB1 and TRPV1 receptors exert opposite modulation on expression of contextual fear conditioning. Neuropharmacology 103, 257269.CrossRefGoogle ScholarPubMed
Uliana, DL, Antero, LS, Borges-Assis, AB, Rosa, J, Vila-Verde, C, Lisboa, SF and Resstel, LB (2020) Differential modulation of the contextual conditioned emotional response by CB1 and TRPV1 receptors in the ventromedial prefrontal cortex: possible involvement of NMDA/nitric oxide-related mechanisms. Journal of Psychopharmacology 34(9), 10431055.CrossRefGoogle ScholarPubMed
Wilson-Poe, AR, Morgan, MM, Aicher, SA and Hegarty, DM (2012) Distribution of CB1 cannabinoid receptors and their relationship with mu-opioid receptors in the rat periaqueductal gray. Neuroscience 213, 191200.CrossRefGoogle ScholarPubMed
Wilson, RI and Nicoll, RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410(6828), 588592.CrossRefGoogle ScholarPubMed
Wu, Y, Liu, Q, Guo, B, Ye, F, Ge, J and Xue, L (2020) BDNF activates postsynaptic trkB receptors to induce endocannabinoid release and inhibit presynaptic calcium influx at a calyx-type synapse. The Journal of Neuroscience 40(42), 80708087.CrossRefGoogle Scholar
Yang, K, Lei, G, Xie, Y-F, MacDonald, JF and Jackson, MF (2014) Differential regulation of NMDAR and NMDAR-mediated metaplasticity by anandamide and 2-AG in the hippocampus. Hippocampus 24(12), 16011614.CrossRefGoogle ScholarPubMed
Yeh, ML, Selvam, R and Levine, ES (2017) BDNF-induced endocannabinoid release modulates neocortical glutamatergic neurotransmission. Synapse 71(5).CrossRefGoogle ScholarPubMed
Zhang, D, Saraf, A, Kolasa, T, Bhatia, P, Zheng, GZ, Patel, M, Lannoye, GS, Richardson, P, Stewart, A, Rogers, JC, Brioni, JD and Surowy, CS (2007) Fatty acid amide hydrolase inhibitors display broad selectivity and inhibit multiple carboxylesterases as off-targets. Neuropharmacology 52(4), 10951105.CrossRefGoogle ScholarPubMed
Zhao, R and Tsang, SY (2017) Versatile roles of intracellularly located TRPV1 channel. Journal of Cellular Physiology 232(8), 19571965.CrossRefGoogle ScholarPubMed
Zschenderlein, C, Gebhardt, C, von Bohlen und Halbach, O, Kulisch, C, Albrecht, D, Baccei, ML (2011) Capsaicin-induced changes in LTP in the lateral amygdala are mediated by TRPV1. PloS one 6(1), e16116.CrossRefGoogle ScholarPubMed
Zygmunt, PM, Petersson, J, Andersson, DA, Chuang, H, Sørgård, M, Di Marzo, V, Julius, D and Högestätt, ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400(6743), 452457.CrossRefGoogle ScholarPubMed