Exportar registro bibliográfico


Tempering aversive/traumatic memories with cannabinoids: a review of evidence from animal and human studies (2019)

  • Authors:
  • Schools: FCFRP; FMRP
  • DOI: 10.1007/s00213-018-5127-x
  • Keywords: Stress; Anxiety; Endocannabinoid; Cannabidiol; Extinction
  • Agências de fomento:
  • Language: Inglês
  • Imprenta:
  • Source:
  • Online source accessDOI
    Informações sobre o DOI: 10.1007/s00213-018-5127-x (Fonte: oaDOI API)
    • Este periódico é de assinatura
    • Este artigo NÃO é de acesso aberto
    • Cor do Acesso Aberto: closed

    How to cite
    A citação é gerada automaticamente e pode não estar totalmente de acordo com as normas

    • ABNT

      LISBOA, Sabrina Francesca de Souza; VILA-VERDE, Carla; ROSA, Jéssica; et al. Tempering aversive/traumatic memories with cannabinoids: a review of evidence from animal and human studies. Psychopharmacology, Heidelberg, v. 236, n. 1, p. 201-226, 2019. Disponível em: < https://doi.org/10.1007/s00213-018-5127-x > DOI: 10.1007/s00213-018-5127-x.
    • APA

      Lisboa, S. F. de S., Vila-Verde, C., Rosa, J., Uliana, D. L. M., Stern, C. A. J., Bertoglio, L. J., et al. (2019). Tempering aversive/traumatic memories with cannabinoids: a review of evidence from animal and human studies. Psychopharmacology, 236( 1), 201-226. doi:10.1007/s00213-018-5127-x
    • NLM

      Lisboa SF de S, Vila-Verde C, Rosa J, Uliana DLM, Stern CAJ, Bertoglio LJ, Resstel LBM, Guimarães FS. Tempering aversive/traumatic memories with cannabinoids: a review of evidence from animal and human studies [Internet]. Psychopharmacology. 2019 ; 236( 1): 201-226.Available from: https://doi.org/10.1007/s00213-018-5127-x
    • Vancouver

      Lisboa SF de S, Vila-Verde C, Rosa J, Uliana DLM, Stern CAJ, Bertoglio LJ, Resstel LBM, Guimarães FS. Tempering aversive/traumatic memories with cannabinoids: a review of evidence from animal and human studies [Internet]. Psychopharmacology. 2019 ; 236( 1): 201-226.Available from: https://doi.org/10.1007/s00213-018-5127-x

    Referências citadas na obra
    Abush H, Akirav I (2013) Cannabinoids ameliorate impairments induced by chronic stress to synaptic plasticity and short-term memory. Neuropsychopharmacology 38:1521–1534
    Aguiar DC, Moreira FA, Terzian AL, Fogaça MV, Lisboa SF, Wotjak CT, Guimaraes FS (2014) Modulation of defensive behavior by transient receptor potential vanilloid type-1 (TRPV1) channels. Neurosci Biobehav Rev 46(Pt 3):418–428
    Aisenberg N, Serova L, Sabban EL, Akirav I (2017) The effects of enhancing endocannabinoid signaling and blocking corticotrophin releasing factor receptor in the amygdala and hippocampus on the consolidation of a stressful event. Eur Neuropsychopharmacol 27:913–927
    Akirav I, Maroun M (2007) The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plasticity 2007:30873
    Alves FH, Gomes FV, Reis DG, Crestani CC, Correa FM, Guimaraes FS, Resstel LB (2013) Involvement of the insular cortex in the consolidation and expression of contextual fear conditioning. Eur J Neurosci 38:2300–2307
    Amstadter AB, Nugent NR, Koenen KC (2009) Genetics of PTSD: fear conditioning as a model for future research. Psychiatr Ann 39:358–367
    Antov MI, Wolk C, Stockhorst U (2013) Differential impact of the first and second wave of a stress response on subsequent fear conditioning in healthy men. Biol Psychol 94:456–468
    Araque A, Castillo PE, Manzoni OJ, Tonini R (2017) Synaptic functions of endocannabinoid signaling in health and disease. Neuropharmacology 124:13–24
    Ashton JC, Smith PF, Darlington CL (2008) The effect of delta 9-tetrahydrocannabinol on the extinction of an adverse associative memory. Pharmacology 81:18–20
    Auclair N, Otani S, Soubrie P, Crepel F (2000) Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 83:3287–3293
    Baldi E, Bucherelli C (2015) Brain sites involved in fear memory reconsolidation and extinction of rodents. Neurosci Biobehav Rev 53:160–190
    Barros D, Ramirez M, Izquierdo I (2005) Modulation of working, short- and long-term memory by nicotinic receptors in the basolateral amygdala in rats. Neurobiol Learn Mem 83:113–118
    Bedse G, Bluett RJ, Patrick TA, Romness NK, Gaulden AD, Kingsley PJ, Plath N, Marnett LJ, Patel S (2018) Therapeutic endocannabinoid augmentation for mood and anxiety disorders: comparative profiling of FAAH, MAGL and dual inhibitors. Transl Psychiatry 8:92
    Bedse G, Hartley ND, Neale E, Gaulden AD, Patrick TA, Kingsley PJ, Uddin MJ, Plath N, Marnett LJ, Patel S (2017) Functional redundancy between canonical endocannabinoid signaling systems in the modulation of anxiety. Biol Psychiatry 82:488–499
    Bennett MR, Arnold J, Hatton SN, Lagopoulos J (2017) Regulation of fear extinction by long-term depression: the roles of endocannabinoids and brain derived neurotrophic factor. Behav Brain Res 319:148–164
    Bentz D, Michael T, Wilhelm FH, Hartmann FR, Kunz S, von Rohr IR, de Quervain DJ (2013) Influence of stress on fear memory processes in an aversive differential conditioning paradigm in humans. Psychoneuroendocrinology 38:1186–1197
    Besnard A, Sahay A (2016) Adult hippocampal neurogenesis, fear generalization, and stress. Neuropsychopharmacology 41:24–44
    Bitencourt RM, Pamplona FA, Takahashi RN (2008) Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. Eur Neuropsychopharmacol 18:849–859
    Bitencourt RM, Pamplona FA, Takahashi RN (2014) Corticosteroid-endocannabinoid loop supports decrease of fear-conditioned response in rats. Eur Neuropsychopharmacol : J Eur Coll Neuropsychopharmacol 24:1091–1102
    Blechert J, Michael T, Vriends N, Margraf J, Wilhelm FH (2007) Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behav Res Ther 45:2019–2033
    Bluett RJ, Baldi R, Haymer A, Gaulden AD, Hartley ND, Parrish WP, Baechle J, Marcus DJ, Mardam-Bey R, Shonesy BC, Uddin MJ, Marnett LJ, Mackie K, Colbran RJ, Winder DG, Patel S (2017) Endocannabinoid signalling modulates susceptibility to traumatic stress exposure. Nat Commun 8:14782
    Bojnik E, Turunc E, Armagan G, Kanit L, Benyhe S, Yalcin A, Borsodi A (2012) Changes in the cannabinoid (CB1) receptor expression level and G-protein activation in kainic acid induced seizures. Epilepsy Res 99:64–68
    Bolles RC, Collier AC (1976) The effect of predictive cues on freezing in rats. Anim Learn Behav 4:6–8
    Bonn-Miller MO, Boden MT, Vujanovic AA, Drescher KD (2013) Prospective investigation of the impact of cannabis use disorders on posttraumatic stress disorder symptoms among veterans in residential treatment. Psychol Trauma 5:193–200
    Bowers ME, Ressler KJ (2015) An overview of translationally informed treatments for posttraumatic stress disorder: animal models of Pavlovian fear conditioning to human clinical trials. Biol Psychiatry 78:E15–E27
    Bremner JD, Vermetten E, Schmahl C, Vaccarino V, Vythilingam M, Afzal N, Grillon C, Charney DS (2005) Positron emission tomographic imaging of neural correlates of a fear acquisition and extinction paradigm in women with childhood sexual-abuse-related post-traumatic stress disorder. Psychol Med 35:791–806
    Bremner JD, Vythilingam M, Vermetten E, Southwick SM, McGlashan T, Nazeer A, Khan S, Vaccarino LV, Soufer R, Garg PK, Ng CK, Staib LH, Duncan JS, Charney DS (2003) MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. Am J Psychiatry 160:924–932
    Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A (2012) Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 76:790–803
    Brunet A, Orr SP, Tremblay J, Robertson K, Nader K, Pitman RK (2008) Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. J Psychiatr Res 42:503–506
    Bryant RA, Felmingham KL, Kemp AH, Barton M, Peduto AS, Rennie C, Gordon E, Williams LM (2005) Neural networks of information processing in posttraumatic stress disorder: a functional magnetic resonance imaging study. Biol Psychiatry 58:111–118
    Bush DE, Caparosa EM, Gekker A, Ledoux J (2010) Beta-adrenergic receptors in the lateral nucleus of the amygdala contribute to the acquisition but not the consolidation of auditory fear conditioning. Front Behav Neurosci 4:154
    Campos AC, Ferreira FR, Guimaraes FS (2012) Cannabidiol blocks long-lasting behavioral consequences of predator threat stress: possible involvement of 5HT1A receptors. J Psychiatr Res 46:1501–1510
    Cannich A, Wotjak CT, Kamprath K, Hermann H, Lutz B, Marsicano G (2004) CB1 cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice. Learn Mem 11:625–632
    Carobrez AP, Bertoglio LJ (2005) Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 29:1193–1205
    Carrion VG, Weems CF, Eliez S, Patwardhan A, Brown W, Ray RD, Reiss AL (2001) Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder. Biol Psychiatry 50:943–951
    Cavener VS, Gaulden A, Pennipede D, Jagasia P, Uddin J, Marnett LJ, Patel S (2018) Inhibition of diacylglycerol lipase impairs fear extinction in mice. Front Neurosci 12:479
    Chhatwal JP, Davis M, Maguschak KA, Ressler KJ (2005) Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 30:516–524
    Chhatwal JP, Gutman AR, Maguschak KA, Bowser ME, Yang Y, Davis M, Ressler KJ (2009) Functional interactions between endocannabinoid and CCK neurotransmitter systems may be critical for extinction learning. Neuropsychopharmacology 34:509–521
    Chiang KP, Gerber AL, Sipe JC, Cravatt BF (2004) Reduced cellular expression and activity of the P129T mutant of human fatty acid amide hydrolase: evidence for a link between defects in the endocannabinoid system and problem drug use. Hum Mol Genet 13:2113–2119
    Childers SR, Deadwyler SA (1996) Role of cyclic AMP in the actions of cannabinoid receptors. Biochem Pharmacol 52:819–827
    Cohen J (1989) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, New York
    Colgin LL, Moser EI, Moser MB (2008) Understanding memory through hippocampal remapping. Trends Neurosci 31:469–477
    Corcoran KA, Maren S (2001) Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J Neurosci 21:1720–1726
    Czerniawski J, Guzowski JF (2014) Acute neuroinflammation impairs context discrimination memory and disrupts pattern separation processes in hippocampus. J Neurosci 34:12470–12480
    Das RK, Kamboj SK, Ramadas M, Yogan K, Gupta V, Redman E, Curran HV, Morgan CJ (2013) Cannabidiol enhances consolidation of explicit fear extinction in humans. Psychopharmacology 226:781–792
    de Oliveira Alvares L, Pasqualini Genro B, Diehl F, Molina VA, Quillfeldt JA (2008) Opposite action of hippocampal CB1 receptors in memory reconsolidation and extinction. Neuroscience 154:1648–1655
    Deng W, Mayford M, Gage FH (2013) Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. eLife 2:e00312
    Denny CA, Kheirbek MA, Alba EL, Tanaka KF, Brachman RA, Laughman KB, Tomm NK, Turi GF, Losonczy A, Hen R (2014) Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis. Neuron 83:189–201
    Desmedt A, Marighetto A, Piazza PV (2015) Abnormal fear memory as a model for posttraumatic stress disorder. Biol Psychiatry 78:290–297
    Deuker L, Doeller CF, Fell J, Axmacher N (2014) Human neuroimaging studies on the hippocampal CA3 region—integrating evidence for pattern separation and completion. Front Cell Neurosci 8:64
    Dincheva I, Drysdale AT, Hartley CA, Johnson DC, Jing D, King EC, Ra S, Gray JM, Yang R, DeGruccio AM, Huang C, Cravatt BF, Glatt CE, Hill MN, Casey BJ, Lee FS (2015) FAAH genetic variation enhances fronto-amygdala function in mouse and human. Nat Commun 6:6395
    Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci U S A 99:10819–10824
    Do Monte FH, Souza RR, Bitencourt RM, Kroon JA, Takahashi RN (2013) Infusion of cannabidiol into infralimbic cortex facilitates fear extinction via CB1 receptors. Behav Brain Res 250:23–27
    Dubreucq S, Koehl M, Abrous DN, Marsicano G, Chaouloff F (2010) CB1 receptor deficiency decreases wheel-running activity: consequences on emotional behaviours and hippocampal neurogenesis. Exp Neurol 224:106–113
    Dubreucq S, Matias I, Cardinal P, Haring M, Lutz B, Marsicano G, Chaouloff F (2012) Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37:1885–1900
    Egertova M, Giang DK, Cravatt BF, Elphick MR (1998) A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc Biol Sci 265:2081–2085
    Egertová M, Giang DK, Cravatt BF, Elphick MR (1998) A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc Biol Sci 265:2081–2085
    Elzinga BM, Bremner JD (2002) Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? J Affect Disord 70:1–17
    Etkin A, Wager TD (2007) Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder and specific phobia. Am J Psychiatry 164:1476–1488
    Fattore L, Fratta W (2010) How important are sex differences in cannabinoid action? Br J Pharmacol 160:544–548
    Fidelman S, Mizrachi Zer-Aviv T, Lange R, Hillard CJ, Akirav I (2018) Chronic treatment with URB597 ameliorates post-stress symptoms in a rat model of PTSD. Eur Neuropsychopharmacol 28(5):630–642.
    Fiorenza NG, Rosa J, Izquierdo I, Myskiw JC (2012) Modulation of the extinction of two different fear-motivated tasks in three distinct brain areas. Behav Brain Res 232:210–216
    Fitzgerald PJ, Seemann JR, Maren S (2014) Can fear extinction be enhanced? A review of pharmacological and behavioral findings. Brain Res Bull 105:46–60
    Fonzo GA, Simmons AN, Thorp SR, Norman SB, Paulus MP, Stein MB (2010) Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biol Psychiatry 68:433–441
    Ganon-Elazar E, Akirav I (2009) Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. J Neurosci 29:11078–11088
    Ganon-Elazar E, Akirav I (2012) Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress. Neuropsychopharmacology 37:456–466
    Ganon-Elazar E, Akirav I (2013) Cannabinoids and traumatic stress modulation of contextual fear extinction and GR expression in the amygdala-hippocampal-prefrontal circuit. Psychoneuroendocrinology 38:1675–1687
    Garcia R, Spennato G, Nilsson-Todd L, Moreau JL, Deschaux O (2008) Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats. Neurobiol Learn Mem 89:560–566
    Garfinkel SN, Abelson JL, King AP, Sripada RK, Wang X, Gaines LM, Liberzon I (2014) Impaired contextual modulation of memories in PTSD: an fMRI and psychophysiological study of extinction retention and fear renewal. J Neurosci 34:13435–13443
    Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, Pitman RK (2002) Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci 5:1242–1247
    Glover EM, Phifer JE, Crain DF, Norrholm SD, Davis M, Bradley B, Ressler KJ, Jovanovic T (2011) Tools for translational neuroscience: PTSD is associated with heightened fear responses using acoustic startle but not skin conductance measures. Depress Anxiety 28:1058–1066
    Gold AL, Shin LM, Orr SP, Carson MA, Rauch SL, Macklin ML, Lasko NB, Metzger LJ, Dougherty DD, Alpert NM, Fischman AJ, Pitman RK (2011) Decreased regional cerebral blood flow in medial prefrontal cortex during trauma-unrelated stressful imagery in Vietnam veterans with post-traumatic stress disorder. Psychol Med 41:2563–2572
    Goswami S, Cascardi M, Rodriguez-Sierra OE, Duvarci S, Pare D (2010) Impact of predatory threat on fear extinction in Lewis rats. Learn Mem 17:494–501
    Green MK, Rani CS, Joshi A, Soto-Pina AE, Martinez PA, Frazer A, Strong R, Morilak DA (2011) Prenatal stress induces long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress. Neuroscience 192:438–451
    Greer GR, Grob CS, Halberstadt AL (2014) PTSD symptom reports of patients evaluated for the New Mexico Medical Cannabis Program. J Psychoactive Drugs 46:73–77
    Grillon C, Morgan CA 3rd (1999) Fear-potentiated startle conditioning to explicit and contextual cues in Gulf War veterans with posttraumatic stress disorder. J Abnorm Psychol 108:134–142
    Gunduz-Cinar O, MacPherson KP, Cinar R, Gamble-George J, Sugden K, Williams B, Godlewski G, Ramikie TS, Gorka AX, Alapafuja SO, Nikas SP, Makriyannis A, Poulton R, Patel S, Hariri AR, Caspi A, Moffitt TE, Kunos G, Holmes A (2013) Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity. Mol Psychiatry 18:813–823
    Gurvits TV, Shenton ME, Hokama H, Ohta H, Lasko NB, Gilbertson MW, Orr SP, Kikinis R, Jolesz FA, McCarley RW, Pitman RK (1996) Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol Psychiatry 40:1091–1099
    Guthrie RM, Bryant RA (2006) Extinction learning before trauma and subsequent posttraumatic stress. Psychosom Med 68:307–311
    Hariri AR, Gorka A, Hyde LW, Kimak M, Halder I, Ducci F, Ferrell RE, Goldman D, Manuck SB (2009) Divergent effects of genetic variation in endocannabinoid signaling on human threat- and reward-related brain function. Biol Psychiatry 66:9–16
    Hartley CA, Gorun A, Reddan MC, Ramirez F, Phelps EA (2014) Stressor controllability modulates fear extinction in humans. Neurobiol Learn Mem 113:149–156
    Hartley ND, Gunduz-Cinar O, Halladay L, Bukalo O, Holmes A, Patel S (2016) 2-arachidonoylglycerol signaling impairs short-term fear extinction. Transl Psychiatry 6:e749
    Hayes JP, Hayes SM, Mikedis AM (2012) Quantitative meta-analysis of neural activity in posttraumatic stress disorder. Biol Mood & Anxiety Dis 2:9
    Heitland I, Klumpers F, Oosting RS, Evers DJ, Leon Kenemans J, Baas JM (2012) Failure to extinguish fear and genetic variability in the human cannabinoid receptor 1. Transl Psychiatry 2:e162
    Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563–583
    Hill MN, Campolongo P, Yehuda R, Patel S (2018) Integrating endocannabinoid signaling and cannabinoids into the biology and treatment of posttraumatic stress disorder. Neuropsychopharmacology 43:80–102
    Hoffman AN, Lorson NG, Sanabria F, Foster Olive M, Conrad CD (2014) Chronic stress disrupts fear extinction and enhances amygdala and hippocampal Fos expression in an animal model of post-traumatic stress disorder. Neurobiol Learn Mem 112:139–147
    Holmes A, Singewald N (2013) Individual differences in recovery from traumatic fear. Trends Neurosci 36:23–31
    Hou L, Klann E (2004) Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 24:6352–6361
    Izquierdo A, Wellman CL, Holmes A (2006) Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J Neurosci 26:5733–5738
    Izquierdo I, Barros DM, Mello e Souza T, de Souza MM, Izquierdo LA, Medina JH (1998) Mechanisms for memory types differ. Nature 393:635–636
    Izquierdo I, Furini CRG, Myskiw JC (2016) Fear memory. Physiol Rev 96:695–750
    Jackson ED, Payne JD, Nadel L, Jacobs WJ (2006) Stress differentially modulates fear conditioning in healthy men and women. Biol Psychiatry 59:516–522
    Jacob W, Marsch R, Marsicano G, Lutz B, Wotjak CT (2012) Cannabinoid CB1 receptor deficiency increases contextual fear memory under highly aversive conditions and long-term potentiation in vivo. Neurobiol Learn Mem 98:47–55
    Jenniches I, Ternes S, Albayram O, Otte DM, Bach K, Bindila L, Michel K, Lutz B, Bilkei-Gorzo A, Zimmer A (2016) Anxiety, stress, and fear response in mice with reduced endocannabinoid levels. Biol Psychiatry 79:858–868
    Jovanovic T, Kazama A, Bachevalier J, Davis M (2012) Impaired safety signal learning may be a biomarker of PTSD. Neuropharmacology 62:695–704
    Jovanovic T, Norrholm SD, Blanding NQ, Davis M, Duncan E, Bradley B, Ressler KJ (2010) Impaired fear inhibition is a biomarker of PTSD but not depression. Depress Anxiety 27:244–251
    Jovanovic T, Ressler KJ (2010) How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am J Psychiatry 167:648–662
    Kamprath K, Marsicano G, Tang J, Monory K, Bisogno T, Di Marzo V, Lutz B, Wotjak CT (2006) Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 26:6677–6686
    Kamprath K, Plendl W, Marsicano G, Deussing JM, Wurst W, Lutz B, Wotjak CT (2009) Endocannabinoids mediate acute fear adaptation via glutamatergic neurons independently of corticotropin-releasing hormone signaling. Genes Brain Behav 8:203–211
    Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380
    Karstoft KI, Statnikov A, Andersen SB, Madsen T, Galatzer-Levy IR (2015) Early identification of posttraumatic stress following military deployment: application of machine learning methods to a prospective study of Danish soldiers. J Affect Disord 184:170–175
    Kasckow JW, Mulchahey JJ, Geracioti TD Jr (2004) Effects of the vanilloid agonist olvanil and antagonist capsazepine on rat behaviors. Prog Neuro-Psychopharmacol Biol Psychiatry 28:291–295
    Kawahara H, Drew GM, Christie MJ, Vaughan CW (2011) Inhibition of fatty acid amide hydrolase unmasks CB1 receptor and TRPV1 channel-mediated modulation of glutamatergic synaptic transmission in midbrain periaqueductal grey. Br J Pharmacol 163:1214–1222
    Kheirbek MA, Klemenhagen KC, Sahay A, Hen R (2012) Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 15:1613–1620
    Kim J, Alger BE (2010) Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses. Nat Neurosci 13:592–600
    Kishimoto Y, Cagniard B, Yamazaki M, Nakayama J, Sakimura K, Kirino Y, Kano M (2015) Task-specific enhancement of hippocampus-dependent learning in mice deficient in monoacylglycerol lipase, the major hydrolyzing enzyme of the endocannabinoid 2-arachidonoylglycerol. Front Behav Neurosci 9:134
    Kitayama N, Vaccarino V, Kutner M, Weiss P, Bremner JD (2005) Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: a meta-analysis. J Affect Disord 88:79–86
    Klumpers F, Denys D, Kenemans JL, Grillon C, van der Aart J, Baas JM (2012) Testing the effects of Delta9-THC and D-cycloserine on extinction of conditioned fear in humans. J Psychopharmacol 26:471–478
    Knox D, George SA, Fitzpatrick CJ, Rabinak CA, Maren S, Liberzon I (2012) Single prolonged stress disrupts retention of extinguished fear in rats. Learn Mem 19:43–49
    Knox D, Perrine SA, George SA, Galloway MP, Liberzon I (2010) Single prolonged stress decreases glutamate, glutamine, and creatine concentrations in the rat medial prefrontal cortex. Neurosci Lett 480:16–20
    Kobilo T, Hazvi S, Dudai Y (2007) Role of cortical cannabinoid CB1 receptor in conditioned taste aversion memory. Eur J Neurosci 25:3417–3421
    Kong E, Monje FJ, Hirsch J, Pollak DD (2014) Learning not to fear: neural correlates of learned safety. Neuropsychopharmacology 39:515–527
    Korem N, Akirav I (2014) Cannabinoids prevent the effects of a footshock followed by situational reminders on emotional processing. Neuropsychopharmacology 39:2709–2722
    Korem N, Lange R, Hillard CJ, Akirav I (2017) Role of beta-catenin and endocannabinoids in the nucleus accumbens in extinction in rats exposed to shock and reminders. Neuroscience 357:285–294
    Kroes MC, Tendolkar I, van Wingen GA, van Waarde JA, Strange BA, Fernandez G (2014) An electroconvulsive therapy procedure impairs reconsolidation of episodic memories in humans. Nat Neurosci 17:204–206
    Kuhnert S, Meyer C, Koch M (2013) Involvement of cannabinoid receptors in the amygdala and prefrontal cortex of rats in fear learning, consolidation, retrieval and extinction. Behav Brain Res 250:274–284
    LaLumiere RT, McGaugh JL, McIntyre CK (2017) Emotional modulation of learning and memory: pharmacological implications. Pharmacol Rev 69:236–255
    Laricchiuta D, Centonze D, Petrosini L (2013) Effects of endocannabinoid and endovanilloid systems on aversive memory extinction. Behav Brain Res 256:101–107
    LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184
    Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961–966
    Liberzon I, Krstov M, Young EA (1997) Stress-restress: effects on ACTH and fast feedback. Psychoneuroendocrinology 22:443–453
    Liberzon I, Taylor SF, Amdur R, Jung TD, Chamberlain KR, Minoshima S, Koeppe RA, Fig LM (1999) Brain activation in PTSD in response to trauma-related stimuli. Biol Psychiatry 45:817–826
    Lim J, Igarashi M, Jung KM, Butini S, Campiani G, Piomelli D (2016) Endocannabinoid modulation of predator stress-induced long-term anxiety in rats. Neuropsychopharmacology 41:1329–1339
    Lin HC, Mao SC, Chen PS, Gean PW (2008) Chronic cannabinoid administration in vivo compromises extinction of fear memory. Learn Mem 15:876–884
    Lin HC, Mao SC, Su CL, Gean PW (2009) The role of prefrontal cortex CB1 receptors in the modulation of fear memory. Cereb Cortex 19:165–175
    Linnman C, Zeffiro TA, Pitman RK, Milad MR (2011) An fMRI study of unconditioned responses in post-traumatic stress disorder. Biol Mood & Anxiety Dis 1:8
    Lisboa SF, Reis DG, da Silva AL, Correa FM, Guimaraes FS, Resstel LB (2010) Cannabinoid CB1 receptors in the medial prefrontal cortex modulate the expression of contextual fear conditioning. Int J Neuropsychopharmacol 13:1163–1173
    Lisboa SF, Gomes FV, Silva AL, Uliana DL, Camargo LH, Guimaraes FS, Cunha FQ, Joca SR, Resstel LB (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. Int J Neuropsychopharmacol 18(8). https://doi.org/10.1093/ijnp/pyv005
    Lisboa SF, Niraula A, Resstel LB, Guimaraes FS, Godbout JP, Sheridan JF (2018) Repeated social defeat-induced neuroinflammation, anxiety-like behavior and resistance to fear extinction were attenuated by the cannabinoid receptor agonist WIN55,212-2. Neuropsychopharmacology 43:1924–1933
    Llorente-Berzal A, Terzian AL, di Marzo V, Micale V, Viveros MP, Wotjak CT (2015) 2-AG promotes the expression of conditioned fear via cannabinoid receptor type 1 on GABAergic neurons. Psychopharmacology 232:2811–2825
    Lopez J, Gamache K, Schneider R, Nader K (2015) Memory retrieval requires ongoing protein synthesis and NMDA receptor activity-mediated AMPA receptor trafficking. J Neurosci 35:2465–2475
    Lopresto D, Schipper P, Homberg JR (2016) Neural circuits and mechanisms involved in fear generalization: implications for the pathophysiology and treatment of posttraumatic stress disorder. Neurosci Biobehav Rev 60:31–42
    Lu AT, Ogdie MN, Jarvelin MR, Moilanen IK, Loo SK, McCracken JT, McGough JJ, Yang MH, Peltonen L, Nelson SF, Cantor RM, Smalley SL (2008) Association of the cannabinoid receptor gene (CNR1) with ADHD and post-traumatic stress disorder. Am J Med Gen Part B, Neuropsychiatr Genet 147B:1488–1494
    Lundqvist T, Jonsson S, Warkentin S (2001) Frontal lobe dysfunction in long-term cannabis users. Neurotoxicol Teratol 23:437–443
    Mahan AL, Ressler KJ (2012) Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci 35:24–35
    Manwell LA, Satvat E, Lang ST, Allen CP, Leri F, Parker LA (2009) FAAH inhibitor, URB-597, promotes extinction and CB(1) antagonist, SR141716, inhibits extinction of conditioned aversion produced by naloxone-precipitated morphine withdrawal, but not - extinction of conditioned preference produced by morphine in rats. Pharmacol Biochem Behav 94:154–162
    Manwell LA, Mallet PE (2015) Comparative effects of pulmonary and parenteral Delta(9)-tetrahydrocannabinol exposure on extinction of opiate-induced conditioned aversion in rats. Psychopharmacology 232:1655–1665
    Maren S, Holmes A (2016) Stress and fear extinction. Neuropsychopharmacology 41:58–79
    Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417–428
    Marsch R, Foeller E, Rammes G, Bunck M, Kössl M, Holsboer F, Zieglgänsberger W, Landgraf R, Lutz B, Wotjak CT (2007) Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 27:832–839
    Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530–534
    Matsumoto M, Togashi H, Konno K, Koseki H, Hirata R, Izumi T, Yamaguchi T, Yoshioka M (2008) Early postnatal stress alters the extinction of context-dependent conditioned fear in adult rats. Pharmacol Biochem Behav 89:247–252
    Mayer TA, Matar MA, Kaplan Z, Zohar J, Cohen H (2014) Blunting of the HPA-axis underlies the lack of preventive efficacy of early post-stressor single-dose Delta-9-tetrahydrocannabinol (THC). Pharmacol Biochem Behav 122:307–318
    Mayo LM, Asratian A, Linde J, Holm L, Natt D, Augier G, Stensson N, Vecchiarelli HA, Balsevich G, Aukema RJ, Ghafouri B, Spagnolo PA, Lee FS, Hill MN, Heilig M (2018) Protective effects of elevated anandamide on stress and fear-related behaviors: translational evidence from humans and mice. Mol Psychiatry. https://doi.org/10.1038/s41380-018-0215-1
    McEwen BS (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105–122
    McGaugh JL, Izquierdo I (2000) The contribution of pharmacology to research on the mechanisms of memory formation. Trends Pharmacol Sci 21:208–210
    McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205–210
    McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317:94–99
    Meloni EG, Gillis TE, Manoukian J, Kaufman MJ (2014) Xenon impairs reconsolidation of fear memories in a rat model of post-traumatic stress disorder (PTSD). PLoS One 9:e106189
    Mendez P, Stefanelli T, Flores CE, Muller D, Luscher C (2018) Homeostatic plasticity in the hippocampus facilitates memory extinction. Cell Rep 22:1451–1461
    Merz CJ, Hamacher-Dang TC, Wolf OT (2014) Exposure to stress attenuates fear retrieval in healthy men. Psychoneuroendocrinology 41:89–96
    Milad MR, Igoe SA, Lebron-Milad K, Novales JE (2009a) Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience 164:887–895
    Milad MR, Orr SP, Lasko NB, Chang Y, Rauch SL, Pitman RK (2008) Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J Psychiatr Res 42:515–520
    Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, Zeidan MA, Handwerger K, Orr SP, Rauch SL (2009b) Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66:1075–1082
    Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63:129–151
    Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL (2007) A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry 62:1191–1194
    Milad MR, Rauch SL, Pitman RK, Quirk GJ (2006) Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 73:61–71
    Milad MR, Zeidan MA, Contero A, Pitman RK, Klibanski A, Rauch SL, Goldstein JM (2010) The influence of gonadal hormones on conditioned fear extinction in healthy humans. Neuroscience 168:652–658
    Miracle AD, Brace MF, Huyck KD, Singler SA, Wellman CL (2006) Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 85:213–218
    Mizrachi Zer-Aviv T, Segev A, Akirav I (2016) Cannabinoids and post-traumatic stress disorder: clinical and preclinical evidence for treatment and prevention. Behav Pharmacol 27:561–569
    Morena M, Berardi A, Colucci P, Palmery M, Trezza V, Hill MN, Campolongo P (2018) Enhancing endocannabinoid neurotransmission augments the efficacy of extinction training and ameliorates traumatic stress-induced behavioral alterations in rats. Neuropsychopharmacology 43:1284–1296
    Myskiw JC, Izquierdo I, Furini CRG (2014) Modulation of the extinction of fear learning. Brain Res Bull 105:61–69
    Nader K, Schafe GE, Le Doux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722–726
    Nalloor R, Bunting K, Vazdarjanova A (2011) Predicting impaired extinction of traumatic memory and elevated startle. PLoS One 6:e19760
    Nguyen PT, Schmid CL, Raehal KM, Selley DE, Bohn LM, Sim-Selley LJ (2012) Beta-arrestin2 regulates cannabinoid CB1 receptor signaling and adaptation in a central nervous system region-dependent manner. Biol Psychiatry 71:714–724
    Nieuwenhuis IL, Takashima A (2011) The role of the ventromedial prefrontal cortex in memory consolidation. Behav Brain Res 218:325–334
    Niyuhire F, Varvel SA, Thorpe AJ, Stokes RJ, Wiley JL, Lichtman AH (2007) The disruptive effects of the CB1 receptor antagonist rimonabant on extinction learning in mice are task-specific. Psychopharmacology 191:223–231
    Norrholm SD, Jovanovic T, Olin IW, Sands LA, Karapanou I, Bradley B, Ressler KJ (2011) Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity. Biol Psychiatry 69:556–563
    O'Brien LD, Sticht MA, Mitchnick KA, Limebeer CL, Parker LA, Winters BD (2014) CB1 receptor antagonism in the granular insular cortex or somatosensory area facilitates consolidation of object recognition memory. Neurosci Lett 578:192–196
    Orr SP, Metzger LJ, Lasko NB, Macklin ML, Peri T, Pitman RK (2000) De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder. J Abnorm Psychol 109:290–298
    Orsini CA, Maren S (2012) Neural and cellular mechanisms of fear and extinction memory formation. Neurosci Biobehav Rev 36:1773–1802
    Pamplona FA, Bitencourt RM, Takahashi RN (2008) Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats. Neurobiol Learn Mem 90:290–293
    Pamplona FA, Prediger RD, Pandolfo P, Takahashi RN (2006) The cannabinoid receptor agonist WIN 55,212-2 facilitates the extinction of contextual fear memory and spatial memory in rats. Psychopharmacology 188:641–649
    Pardini M, Krueger F, Koenigs M, Raymont V, Hodgkinson C, Zoubak S, Goldman D, Grafman J (2012) Fatty-acid amide hydrolase polymorphisms and post-traumatic stress disorder after penetrating brain injury. Transl Psychiatry 2:e75
    Parsons RG, Ressler KJ (2013) Implications of memory modulation for post-traumatic stress and fear disorders. Nat Neurosci 16:146–153
    Passie T, Emrich HM, Karst M, Brandt SD, Halpern JH (2012) Mitigation of post-traumatic stress symptoms by Cannabis resin: a review of the clinical and neurobiological evidence. Drug Test Anal 4:649–659
    Patel S, Hill MN, Cheer JF, Wotjak CT, Holmes A (2017) The endocannabinoid system as a target for novel anxiolytic drugs. Neurosci Biobehav Rev 76:56–66
    Patel S, Hillard CJ (2006) Pharmacological evaluation of cannabinoid receptor ligands in a mouse model of anxiety: further evidence for an anxiolytic role for endogenous cannabinoid signaling. J Pharmacol Exp Ther 318:304–311
    Peri T, Ben-Shakhar G, Orr SP, Shalev AY (2000) Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder. Biol Psychiatry 47:512–519
    Perusini JN, Meyer EM, Long VA, Rau V, Nocera N, Avershal J, Maksymetz J, Spigelman I, Fanselow MS (2016) Induction and expression of fear sensitization caused by acute traumatic stress. Neuropsychopharmacology 41:45–57
    Pickens CL, Theberge FR (2014) Blockade of CB1 receptors prevents retention of extinction but does not increase low preincubated conditioned fear in the fear incubation procedure. Behav Pharmacol 25:23–31
    Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873–884
    Pitman RK, Rasmusson AM, Koenen KC, Shin LM, Orr SP, Gilbertson MW, Milad MR, Liberzon I (2012) Biological studies of post-traumatic stress disorder. Nat Rev Neurosci 13:769–787
    Plendl W, Wotjak CT (2010) Dissociation of within- and between-session extinction of conditioned fear. J Neurosci 30:4990–4998
    Prut L, Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463:3–33
    Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56–72
    Rabinak CA, Angstadt M, Lyons M, Mori S, Milad MR, Liberzon I, Phan KL (2014) Cannabinoid modulation of prefrontal-limbic activation during fear extinction learning and recall in humans. Neurobiol Learn Mem 113:125–134
    Rabinak CA, Angstadt M, Sripada CS, Abelson JL, Liberzon I, Milad MR, Phan KL (2013) Cannabinoid facilitation of fear extinction memory recall in humans. Neuropharmacology 64:396–402
    Rabinak CA, Peters C, Marusak HA, Ghosh S, Phan KL (2018a) Effects of acute Delta9-tetrahydrocannabinol on next-day extinction recall is mediated by post-extinction resting-state brain dynamics. Neuropharmacology 143:289–298
    Rabinak CA, Peters C, Elrahal F, Milad M, Rauch S, Phan L, Greenwald M (2018b) 52. Cannabinoid facilitation of fear extinction in posttraumatic stress disorder. 73rd Ann Meet - Soci Biol Psychiatr Meet 83:S21
    Raio CM, Brignoni-Perez E, Goldman R, Phelps EA (2014) Acute stress impairs the retrieval of extinction memory in humans. Neurobiol Learn Mem 112:212–221
    Raio CM, Phelps EA (2015) The influence of acute stress on the regulation of conditioned fear. Neurobiol Stress 1:134–146
    Rauch SL, Shin LM, Phelps EA (2006) Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future. Biol Psychiatry 60:376–382
    Reich CG, Iskander AN, Weiss MS (2013) Cannabinoid modulation of chronic mild stress-induced selective enhancement of trace fear conditioning in adolescent rats. J Psychopharmacol 27:947–955
    Reich CG, Mohammadi MH, Alger BE (2008) Endocannabinoid modulation of fear responses: learning and state-dependent performance effects. J Psychopharmacol 22:769–777
    Resstel LBM, Joca SRL, Guimarães FG, Corrêa FMA (2006) Involvement of medial prefrontal cortex neurons in behavioral and cardiovascular responses to contextual fear conditioning. Neuroscience 143:377–385
    Riebe CJ, Pamplona FA, Kamprath K, Wotjak CT (2012) Fear relief-toward a new conceptual frame work and what endocannabinoids gotta do with it. Neuroscience 204:159–185
    Roche M, O'Connor E, Diskin C, Finn DP (2007) The effect of CB(1) receptor antagonism in the right basolateral amygdala on conditioned fear and associated analgesia in rats. Eur J Neurosci 26:2643–2653
    Roesler R, Schröder N (2011) Cognitive enhancers: focus on modulatory signaling influencing memory consolidation. Pharmacol Biochem Behav 99:155–163
    Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10:423–433
    Rosenkranz JA, Venheim ER, Padival M (2010) Chronic stress causes amygdala hyperexcitability in rodents. Biol Psychiatry 67:1128–1136
    Ross DA, Arbuckle MR, Travis MJ, Dwyer JB, van Schalkwyk GI, Ressler KJ (2017) An integrated neuroscience perspective on formulation and treatment planning for posttraumatic stress disorder: an educational review. JAMA Psychiatry 74:407–415
    Rougemont-Bucking A, Linnman C, Zeffiro TA, Zeidan MA, Lebron-Milad K, Rodriguez-Romaguera J, Rauch SL, Pitman RK, Milad MR (2011) Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neurosci Ther 17:227–236
    Ruehle S, Remmers F, Romo-Parra H, Massa F, Wickert M, Wortge S, Haring M, Kaiser N, Marsicano G, Pape HC, Lutz B (2013) Cannabinoid CB1 receptor in dorsal telencephalic glutamatergic neurons: distinctive sufficiency for hippocampus-dependent and amygdala-dependent synaptic and behavioral functions. J Neurosci 33:10264–10277
    Ruehle S, Rey AA, Remmers F, Lutz B (2012) The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol 26:23–39
    Sachser RM, Crestani AP, Quillfeldt JA, Mello EST, de Oliveira Alvares L (2015) The cannabinoid system in the retrosplenial cortex modulates fear memory consolidation, reconsolidation and extinction. Learn Mem 22:584–588
    Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–470
    Santini E (2004) Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J Neurosci 24:5704–5710
    Sartim AG, Guimaraes FS, Joca SR (2016) Antidepressant-like effect of cannabidiol injection into the ventral medial prefrontal cortex—possible involvement of 5-HT1A and CB1 receptors. Behav Brain Res 303:218–227
    Sbarski B, Akirav I (2018) Chronic exposure to cannabinoids before an emotional trauma may have negative effects on emotional function. Eur Neuropsychopharmacol 28(8):955–969
    Schacht JP, Hutchison KE, Filbey FM (2012) Associations between cannabinoid receptor-1 (CNR1) variation and hippocampus and amygdala volumes in heavy cannabis users. Neuropsychopharmacology 37:2368–2376
    Schiller D, Monfils MH, Raio CM, Johnson DC, Ledoux JE, Phelps EA (2010) Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463:49–53
    Segev A, Rubin AS, Abush H, Richter-Levin G, Akirav I (2014) Cannabinoid receptor activation prevents the effects of chronic mild stress on emotional learning and LTP in a rat model of depression. Neuropsychopharmacology 39:919–933
    Segev A, Korem N, Mizrachi Zer-Aviv T, Abush H, Lange R, Sauber G, Hillard CJ, Akirav I (2018) Role of endocannabinoids in the hippocampus and amygdala in emotional memory and plasticity. Neuropsychopharmacol : Off Publ Am Coll Neuropsychopharmacol 43:2017–2027
    Shin LM, Bush G, Milad MR, Lasko NB, Brohawn KH, Hughes KC, Macklin ML, Gold AL, Karpf RD, Orr SP, Rauch SL, Pitman RK (2011) Exaggerated activation of dorsal anterior cingulate cortex during cognitive interference: a monozygotic twin study of posttraumatic stress disorder. Am J Psychiatry 168:979–985
    Shin LM, Handwerger K (2009) Is posttraumatic stress disorder a stress-induced fear circuitry disorder? J Trauma Stress 22:409–415
    Shin LM, Lasko NB, Macklin ML, Karpf RD, Milad MR, Orr SP, Goetz JM, Fischman AJ, Rauch SL, Pitman RK (2009) Resting metabolic activity in the cingulate cortex and vulnerability to posttraumatic stress disorder. Arch Genet Psychiatry 66:1099–1107
    Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35:169–191
    Shin LM, McNally RJ, Kosslyn SM, Thompson WL, Rauch SL, Alpert NM, Metzger LJ, Lasko NB, Orr SP, Pitman RK (1999) Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related PTSD: a PET investigation. Am J Psychiatry 156:575–584
    Shors TJ (2001) Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol Learn Mem 75:10–29
    Shors TJ, Weiss C, Thompson RF (1992) Stress-induced facilitation of classical conditioning. Science 257:537–539
    Shoshan N, Segev A, Abush H, Mizrachi Zer-Aviv T, Akirav I (2017) Cannabinoids prevent the differential long-term effects of exposure to severe stress on hippocampal- and amygdala-dependent memory and plasticity. Hippocampus 27:1093–1109
    Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529–538
    Sim LJ, Hampson RE, Deadwyler SA, Childers SR (1996) Effects of chronic treatment with delta9-tetrahydrocannabinol on cannabinoid-stimulated [35S]GTPgammaS autoradiography in rat brain. J Neurosci 16:8057–8066
    Simmons AN, Paulus MP, Thorp SR, Matthews SC, Norman SB, Stein MB (2008) Functional activation and neural networks in women with posttraumatic stress disorder related to intimate partner violence. Biol Psychiatry 64:681–690
    Simone JJ, Green MR, Hodges TE, McCormick CM (2015a) Differential effects of CB1 receptor agonism in behavioural tests of unconditioned and conditioned fear in adult male rats. Behav Brain Res 279:9–16
    Simone JJ, Malivoire BL, McCormick CM (2015b) Effects of CB1 receptor agonism and antagonism on behavioral fear and physiological stress responses in adult intact, ovariectomized, and estradiol-replaced female rats. Neuroscience 306:123–137
    Singewald N, Schmuckermair C, Whittle N, Holmes A, Ressler KJ (2015) Pharmacology of cognitive enhancers for exposure-based therapy of fear, anxiety and trauma-related disorders. Pharmacol Ther 149:150–190
    Smart D, Jerman JC (2000) Anandamide: an endogenous activator of the vanilloid receptor. Trends Pharmacol Sci 21:134
    Song C, Stevenson CW, Guimaraes FS, Lee JL (2016) Bidirectional effects of cannabidiol on contextual fear memory extinction. Front Pharmacol 7:493
    Spagnolo PA, Ramchandani VA, Schwandt ML, Kwako LE, George DT, Mayo LM, Hillard CJ, Heilig M (2016) FAAH gene variation moderates stress response and symptom severity in patients with posttraumatic stress disorder and comorbid alcohol dependence. Alcohol Clin Exp Res 40:2426–2434
    Starowicz K, Maione S, Cristino L, Palazzo E, Marabese I, Rossi F, de Novellis V, Di Marzo V (2007) Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. J Neurosci 27:13739–13749
    Steenkamp MM, Blessing EM, Galatzer-Levy IR, Hollahan LC, Anderson WT (2017) Marijuana and other cannabinoids as a treatment for posttraumatic stress disorder: a literature review. Depress Anxiety 34:207–216
    Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24:4787–4795
    Suvrathan A, Bennur S, Ghosh S, Tomar A, Anilkumar S, Chattarji S (2014) Stress enhances fear by forming new synapses with greater capacity for long-term potentiation in the amygdala. Philos Trans R Soc Lond Ser B Biol Sci 369:20130151
    Szapiro G, Galante JM, Barros DM, Levi de Stein M, Vianna MRM, Izquierdo LA, Izquierdo I, Medina JH (2002) Molecular mechanisms of memory retrieval. Neurochem Res 27:1491–1498
    Terzian AL, dos Reis DG, Guimaraes FS, Correa FM, Resstel LB (2014) Medial prefrontal cortex transient receptor potential vanilloid type 1 (TRPV1) in the expression of contextual fear conditioning in Wistar rats. Psychopharmacology 231:149–157
    Terzian AL, Drago F, Wotjak CT, Micale V (2011) The dopamine and cannabinoid interaction in the modulation of emotions and cognition: assessing the role of cannabinoid CB1 receptor in neurons expressing dopamine D1 receptors. Front Behav Neurosci 5:49
    Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM (2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135:162–168
    Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393–411
    Uliana DL, Hott SC, Lisboa SF, Resstel LBM (2016) Dorsolateral periaqueductal gray matter CB1 and TRPV1 receptors exert opposite modulation on expression of contextual fear conditioning. Neuropharmacology 103:257–269
    van Rooij SJ, Kennis M, Vink M, Geuze E (2016) Predicting treatment outcome in PTSD: a longitudinal functional MRI study on trauma-unrelated emotional processing. Neuropsychopharmacology 41:1156–1165
    VanElzakker MB, Dahlgren MK, Davis FC, Dubois S, Shin LM (2014) From Pavlov to PTSD: the extinction of conditioned fear in rodents, humans, and anxiety disorders. Neurobiol Learn Mem 113:3–18
    Vaughan CW, Connor M, Bagley EE, Christie MJ (2000) Actions of cannabinoids on membrane properties and synaptic transmission in rat periaqueductal gray neurons in vitro. Mol Pharmacol 57:288–295
    Vermetten E, Zhohar J, Krugers HJ (2014) Pharmacotherapy in the aftermath of trauma; opportunities in the ‘golden hours’. Curr Psychiatry Rep 16:455
    Vila-Verde C, Lisboa SF, Uliana DL, Resstel LB, Guimarães FS (2018) F050 - cannabidiol prevents stress-induced impairment of conditioned fear in rats: involvement of serotonergic, cannabinoid and nitrergic systems 11th FENS Forum of Neuroscience, Berlin, Germany
    Vouimba RM, Munoz C, Diamond DM (2006) Differential effects of predator stress and the antidepressant tianeptine on physiological plasticity in the hippocampus and basolateral amygdala. Stress 9:29–40
    Vouimba RM, Yaniv D, Diamond D, Richter-Levin G (2004) Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. Eur J Neurosci 19:1887–1894
    Wang X, Li M, Zhu H, Yu Y, Xu Y, Zhang W, Bian C (2018) Transcriptional regulation involved in fear memory reconsolidation. J Mol Neurosci : MN 65:127–140
    Wang Z, Neylan TC, Mueller SG, Lenoci M, Truran D, Marmar CR, Weiner MW, Schuff N (2010) Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder. Arch Gen Psychiatry 67:296–303
    Wessa M, Flor H (2007) Failure of extinction of fear responses in posttraumatic stress disorder: evidence from second-order conditioning. Am J Psychiatry 164:1684–1692
    Whitaker AM, Gilpin NW, Edwards S (2014) Animal models of post-traumatic stress disorder and recent neurobiological insights. Behav Pharmacol 25:398–409
    Wilber AA, Southwood CJ, Wellman CL (2009) Brief neonatal maternal separation alters extinction of conditioned fear and corticolimbic glucocorticoid and NMDA receptor expression in adult rats. Dev Neurobiol 69:73–87
    Wilkinson ST, Stefanovics E, Rosenheck RA (2015) Marijuana use is associated with worse outcomes in symptom severity and violent behavior in patients with posttraumatic stress disorder. J Clin Psychiatry 76:1174–1180
    Wilson CA, Vazdarjanova A, Terry AV Jr (2013) Exposure to variable prenatal stress in rats: effects on anxiety-related behaviors, innate and contextual fear, and fear extinction. Behav Brain Res 238:279–288
    Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science (New York, NY) 296:678–682
    Woodward SH, Kaloupek DG, Streeter CC, Martinez C, Schaer M, Eliez S (2006) Decreased anterior cingulate volume in combat-related PTSD. Biol Psychiatry 59:582–587
    Xing J, Li J (2007) TRPV1 receptor mediates glutamatergic synaptic input to dorsolateral periaqueductal gray (dl-PAG) neurons. J Neurophysiol 97:503–511
    Yamamoto S, Morinobu S, Fuchikami M, Kurata A, Kozuru T, Yamawaki S (2008) Effects of single prolonged stress and D-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD. Neuropsychopharmacology 33:2108–2116
    Yarnell S (2015) The use of medicinal marijuana for posttraumatic stress disorder: a review of the current literature. Prim Care Companion CNS Disord 17(3). https://doi.org/10.4088/PCC.15r01786
    Yassa MA, Stark CE (2011) Pattern separation in the hippocampus. Trends Neurosci 34:515–525
    Yehuda R, Hoge CW, McFarlane AC, Vermetten E, Lanius RA, Nievergelt CM, Hobfoll SE, Koenen KC, Neylan TC, Hyman SE (2015) Post-traumatic stress disorder. Nat Rev Dis Primers 1:15057
    Zer-Aviv TM, Akirav I (2016) Sex differences in hippocampal response to endocannabinoids after exposure to severe stress. Hippocampus 26:947–957
    Zubedat S, Akirav I (2017) The involvement of cannabinoids and mTOR in the reconsolidation of an emotional memory in the hippocampal-amygdala-insular circuit. European neuropsychopharmacology 27:336–349
    Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sørgård M, Di Marzo V, Julius D, Högestätt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452–457

Digital Library of Intellectual Production of Universidade de São Paulo     2012 - 2022