Failure to extinguish fear and genetic variability in the human cannabinoid receptor 1

Translational Psychiatry

Volumn 2, Issue , 2012, Pages

  Heitland, I ^a,b   Klumpers, F ^a,b   Oosting, R S ^c   Evers, D J J ^a   Leon Kenemans, J ^a,b   Baas, J M P ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

cannabinoid receptor 1; CB1 CNR1; fear extinction; fear potentiated startle

Indexed keywords

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; CANNABINOID RECEPTOR AGONIST;

ADULT; ALLELE; ARTICLE; ARTIFACT; CLINICAL ASSESSMENT; CONDITIONED REFLEX; CONDITIONING; EYELID REFLEX; FEAR; FEMALE; GENE EXPRESSION; GENETIC CODE; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HOMOZYGOTE; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; PROMOTER REGION; RATING SCALE; SINGLE NUCLEOTIDE POLYMORPHISM; STARTLE REFLEX; VIRTUAL REALITY; ANALYSIS OF VARIANCE; ANXIETY; DRUG POTENTIATION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REINFORCEMENT; SEX RATIO;

ALLELES; ANALYSIS OF VARIANCE; ANXIETY; CANNABINOID RECEPTOR AGONISTS; CONDITIONING (PSYCHOLOGY); ENDOCANNABINOIDS; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; GENOTYPE; HUMANS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTOR, CANNABINOID, CB1; SEX DISTRIBUTION; STARTLE REACTION; YOUNG ADULT;

EID: 84873975432     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2012.90     Document Type: Article

References (75)

1. Mineka S, Zinbarg R. Conditioning and ethological models of anxiety disorders: stress-indynamic-context anxiety models. Nebr Symp Motiv 1996; 43: 135-210.
2. Mineka S, Oehlberg K. The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders. Acta Psychol 2008; 127: 567-580.
3. Hofmann SG. Cognitive processes during fear acquisition and extinction in animals and humans: implications for exposure therapy of anxiety disorders. Clin Psychol Rev 2008; 28: 199-210.
4. Myers KM, Davis M. Behavioral and neural analysis of extinction. Neuron 2002; 36: 567-584.
5. Milad MR, Rauch SL, Pitman RK, Quirk GJ. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 2006; 73: 61-71.
6. Kaplan GB, Heinrichs SC, Carey RJ. Treatment of addiction and anxiety using extinction approaches: neural mechanisms and their treatment implications. Pharmacol Biochem Behav 2011; 97: 619-625.
7. Hermans D, Craske MG, Mineka S, Lovibond PF. Extinction in human fear conditioning. Biol Psychiatry 2006; 60: 361-368.
8. Myers KM, Davis M. Mechanisms of fear extinction. Mol Psychiatry 2007; 12: 120-150.
9. Lafenê tre P, Chaouloff F, Marsicano G. The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacol Res 2007; 56: 367-381.
10. Davis M, Walker DL, Miles L, Grillon C. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010; 35: 105-135.
11. Chhatwal JP, Davis M, Maguschak KA, Ressler KJ. Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 2005; 30: 516-524.
12. Pamplona FA, Bitencourt RM, Takahashi RN. Short-and long-term effects of cannabinoids on the extinction of contextual fear memory in rats. Neurobiol Learn Mem 2008; 90: 290-293.
13. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 1990; 87: 1932-1936.
14. Howlett AC. The CB1 cannabinoid receptor in the brain. Neurobiol Dis 1998; 5: 405-416.
15. Howlett AC, Bidaut-Russell M, Devane WA, Melvin LS, Johnson MR, Herkenham M. The cannabinoid receptor: biochemical, anatomical and behavioral characterization. Trends Neurosci 1990; 13: 420-423.
16. Zhang P-W, Ishiguro H, Ohtsuki T, Hess J, Carillo F, Walther D et al. Human cannabinoid receptor 1: 5' exons, candidate regulatory regions, polymorphisms, haplotypes and association with polysubstance abuse. Mol Psychiatry 2004; 9: 916-931.
17. Davies SN, Pertwee RG, Riedel G. Functions of cannabinoid receptors in the hippocampus. Neuropharmacology 2002; 42: 993-1007.
18. Iversen L. Cannabis and the brain. Brain 2003; 126(Pt 6): 1252-1270.
19. Moreira FA, Aguiar DC, Resstel LB, Lisboa SF, Campos AC, Gomes FV et al. Neuroanatomical substrates involved in cannabinoid modulation of defensive responses. J Psychopharmacol 2012; 26: 40-55.
20. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002; 418: 530-534.
21. Bitencourt RM, Pamplona FA, Takahashi RN. Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. Eur Neuropsychopharmacol 2008; 18: 849-859.
22. Pamplona FA, Prediger RD, Pandolfo P, Takahashi RN. The cannabinoid receptor agonist WIN 55,212-2 facilitates the extinction of contextual fear memory and spatial memory in rats. Psychopharmacology 2006; 188: 641-649.
23. Chhatwal JP, Ressler KJ. Modulation of fear and anxiety by the endogenous cannabinoid system. CNS Spectr 2007; 12: 211-220.
24. Graham BM, Milad MR. The study of fear extinction: implications for anxiety disorders. Am J Psychiatry 2011; 168: 1255-1265.
25. Domschke K, Zwanzger P. GABAergic and endocannabinoid dysfunction in anxiety-future therapeutic targets? Curr Pharm Des 2008; 14: 3508-3517.
26. Lutz B. The endocannabinoid system and extinction learning. Mol Neurobiol 2007; 36: 92-101.
27. Davis M. Neural systems involved in fear and anxiety measured with fear-potentiated startle. Am Psychol 2006; 61: 741-756.
28. Davis M, Falls WA, Campeau S, Kim M. Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 1993; 58: 175-198.
29. Grillon C, Baas JMP. A review of the modulation of the startle reflex by affective states and its application in psychiatry. Clin Neurophysiol 2003; 114: 1557-1579.
30. Bradley MM, Moulder B, Lang PJ. When good things go bad: the reflex physiology of defense. Psychol Sci 2005; 16: 468-473.
31. Klumpers F, Heitland I, Oosting RS, Kenemans JL, Baas JM. Genetic variation in serotonin transporter function affects human fear expression indexed by fear-potentiated startle. Biol Psychol 2011; 89: 277-282.
32. Lang PJ, Davis M, Ohman A. Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 2000; 61: 137-159.
33. Lin HC, Mao SC, Chen PS, Gean PW. Chronic cannabinoid administration in vivo compromises extinction of fear memory. Learn Mem 2008; 15: 876-884.
34. Norrholm SD, Jovanovic T, Vervliet B, Myers KM, Davis M, Rothbaum BO et al. Conditioned fear extinction and reinstatement in a human fear-potentiated startle paradigm. Learn Mem 2006; 13: 681-685.
35. Klumpers F, Denys D, Kenemans JL, Grillon C, van der Aart J, Baas JM. Testing the effects of D9-THC and d-cycloserine on extinction of conditioned fear in humans. J Psychopharmacol 2012; 26: 471-478.
36. Vervliet B. Learning and memory in conditioned fear extinction: effects of D-cycloserine. Acta Psychol 2008; 127: 601-613.
37. Guastella AJ, Dadds MR, Lovibond PF, Mitchell P, Richardson RA. randomized controlled trial of the effect of D-cycloserine on exposure therapy for spider fear. J Psychiatr Res 2007; 41: 466-471.
38. Guastella AJ, Lovibond PF, Dadds MR, Mitchell P, Richardson R. A randomized controlled trial of the effect of D-cycloserine on extinction and fear conditioning in humans. Behav Res Ther 2007; 45: 663-672.
39. Cannich A, Wotjak CT, Kamprath K, Hermann H, Lutz B, Marsicano G. CB1 cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice. Learn Mem 2004; 11: 625-632.
40. Kamprath K, Marsicano G, Tang J, Monory K, Bisogno T, Di Marzo V et al. Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 2006; 26: 6677-6686.
41. Hettema JM, Neale MC, Kendler KS. A review and meta-analysis of the genetic epidemiology of anxiety disorders. Am J Psychiatry 2001; 158: 1568-1578.
42. Hettema JM, Annas P, Neale MC, Kendler KS, Fredrikson M. A twin study of the genetics of fear conditioning. Arch Gen Psychiatry 2003; 60: 702-708.
43. Soliman F, Glatt CE, Bath KG, Levita L, Jones RM, Pattwell SS et al. A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 2010; 327: 863-866.
44. Lonsdorf TB, Kalisch R. A review on experimental and clinical genetic associations studies on fear conditioning, extinction and cognitive-behavioral treatment. Transl Psychiatry 2011; 1: e41.
45. Zhang PW, Ishiguro H, Ohtsuki T, Hess J, Carillo F, Walther D et al. Human cannabinoid receptor 1: 5' exons, candidate regulatory regions, polymorphisms, haplotypes and association with polysubstance abuse. Mol Psychiatry 2004; 9: 916-931.
46. Lazary J, Lazary A, Gonda X, Benko A, Molnar E, Hunyady L et al. Promoter variants of the cannabinoid receptor 1 gene (CNR1) in interaction with 5-HTTLPR affect the anxious phenotype. Am J Med Genet B Neuropsychiatr Genet 2009; 150B: 1118-1127.
47. Lu AT, Ogdie MN, Jarvelin MR, Moilanen IK, Loo SK, McCracken JT et al. Association of the cannabinoid receptor gene (CNR1) with ADHD and post-traumatic stress disorder. Am J Med Genet B Neuropsychiatr Genet 2008; 147B: 1488-1494.
48. Domschke K, Dannlowski U, Ohrmann P, Lawford B, Bauer J, Kugel H et al. Cannabinoid receptor 1 (CNR1) gene: impact on antidepressant treatment response and emotion processing in major depression. Eur Neuropsychopharmacol 2008; 18: 751-759.
49. Baas JM, Nugent M, Lissek S, Pine DS, Grillon C. Fear conditioning in virtual reality contexts: a new tool for the study of anxiety. Biol Psychiatry 2004; 55: 1056-1060.
50. Baas JM, van Ooijen L, Goudriaan A, Kenemans JL. Failure to condition to a cue is associated with sustained contextual fear. Acta Psychol 2008; 127: 581-592.
51. Baas JMP. Individual differences in predicting aversive events and modulating contextual anxiety in a context and cue conditioning paradigm. Biol Psychol 2012; e-pub ahead of print.
52. Klumpers F, Raemaekers MA, Ruigrok AN, Hermans EJ, Kenemans JL, Baas JM. Prefrontal mechanisms of fear reduction after threat offset. Biol Psychiatry 2010; 68: 1031-1038.
53. Klumpers F, van Gerven JM, Prinssen EP, Niklson I, Roesch F, Riedel WJ et al. Method development studies for repeatedly measuring anxiolytic drug effects in healthy humans. J Psychopharmacol 2010; 24: 657-666.
54. Blumenthal TD, Cuthbert BN, Filion DL, Hackley S, Lipp OV, van Boxtel A. Committee report: Guidelines for human startle eyeblink electromyographic studies. Psychophysiology 2005; 42: 1-15.
55. Bocker KB, Baas JM, Kenemans JL, Verbaten MN. Differences in startle modulation during instructed threat and selective attention. Biol Psychol 2004; 67: 343-358.
56. Lukkes J, Vuong S, Scholl J, Oliver H, Forster G. Corticotropin-releasing factor receptor antagonism within the dorsal raphe nucleus reduces social anxiety-like behavior after earlylife social isolation. J Neurosci 2009; 29: 9955-9960.
57. Costa PT, McCrae RR. NEO-PI-R Professional Manual. Psychological Assessment ResourcesOdessa, FL, 1992.
58. Cohen J. Statistical power analysis for the behavioral sciences. Erlbaum: Hillsdale, NJ, 1988.
59. Grillon C, Davis M. Fear-potentiated startle conditioning in humans: explicit and contextual cue conditioning following paired versus unpaired training. Psychophysiology 1997; 34: 451-458.
60. Charney DS. Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress. Am J Psychiatry 2004; 161: 195-216.
61. Hill MN, Gorzalka BB. The endocannabinoid system and the treatment of mood and anxiety disorders. CNS Neurol Disord Drug Targets 2009; 8: 451-458.
62. Schlicker E, Kathmann M. Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 2001; 22: 565-572.
63. Kamprath K, Wotjak CT. Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 2004; 11: 770-786.
64. Plendl W, Wotjak CT. Dissociation of within-and between-session extinction of conditioned fear. J Neurosci 2010; 30: 4990-4998.
65. Lonsdorf TB, Weike AI, Nikamo P, Schalling M, Hamm AO, Ohman A. Genetic gating of human fear learning and extinction: possible implications for gene-environment interaction in anxiety disorder. Psychol Sci 2009; 20: 198-206.
66. Schinka JA, Busch RM, Robichaux-Keene N. A meta-analysis of the association between the serotonin transporter gene polymorphism (5-HTTLPR) and trait anxiety. Mol Psychiatry 2004; 9: 197-202.
67. Hofmann SG. Enhancing exposure-based therapy from a translational research perspective. Behav Res Ther 2007; 45: 1987-2001.
68. Bergamaschi MM, Queiroz RH, Chagas MH, de Oliveira DC, De Martinis BS, Kapczinski F et al. Cannabidiol reduces the anxiety induced by simulated public speaking in treatmentnaive social phobia patients. Neuropsychopharmacology 2011; 36: 1219-1226.
69. Crippa JA, Derenusson GN, Ferrari TB, Wichert-Ana L, Duran FL, Martin-Santos R et al. Neural basis of anxiolytic effects of cannabidiol (CBD) in generalized social anxiety disorder: a preliminary report. J Psychopharmacol 2011; 25: 121-130.
70. Fraser GA. The use of a synthetic cannabinoid in the management of treatmentresistant nightmares in posttraumatic stress disorder (PTSD). CNS Neurosci Ther 2009; 15: 84-88.
71. Alonso J, Angermeyer MC, Bernert S, Bruffaerts R, Brugha TS, Bryson H et al. Prevalence of mental disorders in Europe: results from the European Study of the Epidemiology of Mental Disorders (ESEMeD) project. Acta Psychiatr Scand Suppl 2004 21-27.
72. Deacon BJ, Abramowitz JS. Cognitive and behavioral treatments for anxiety disorders: a review of meta-analytic findings. J Clin Psychol 2004; 60: 429-441.
73. Mitte K, Noack P, Steil R, Hautzinger M. A meta-analytic review of the efficacy of drug treatment in generalized anxiety disorder. J Clin Psychopharmacol 2005; 25: 141-150.
74. Schruers K, Koning K, Luermans J, Haack MJ, Griez E. Obsessive-compulsive disorder: a critical review of therapeutic perspectives. Acta Psychiatr Scand 2005; 111: 261-271.
75. Westen D, Morrison K. A multidimensional meta-analysis of treatments for depression, panic, and generalized anxiety disorder: an empirical examination of the status of empirically supported therapies. J Consult Clin Psychol 2001; 69: 875-899.