Pharmacological facilitation of fear extinction and the search for adjunct treatments for anxiety disorders - the case of yohimbine

Trends in Pharmacological Sciences

Volumn 31, Issue 1, 2010, Pages 2-7

  Holmes, Andrew ^a   Quirk, Gregory J ^b  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; ATIPAMEZOLE; CYCLOSERINE; DOPAMINE 2 RECEPTOR; PLACEBO; PROPRANOLOL; SEROTONIN 1A RECEPTOR; YOHIMBINE;

ANXIETY DISORDER; ARTICLE; CLAUSTROPHOBIA; CONDITIONED REFLEX; DRUG EFFICACY; DRUG POTENCY; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; DRUG TARGETING; FEAR; HUMAN; LONG TERM EXPOSURE; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; REINFORCEMENT; SINGLE DRUG DOSE; SYSTEMIC THERAPY; THERAPY EFFECT;

ADRENERGIC ALPHA-ANTAGONISTS; ANIMALS; ANXIETY DISORDERS; BEHAVIOR, ANIMAL; EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; MICE; RECEPTORS, ADRENERGIC, ALPHA-2; YOHIMBINE;

EID: 72749089698     PISSN: 01656147     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tips.2009.10.003     Document Type: Article

References (70)

1. Pavlov I.P. Conditioned reflexes (1927), Oxford University Press
2. Quirk G.J., and Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacol. 33 (2008) 56-72
3. Quirk G.J., and Beer J.S. Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr. Opin. Neurobiol. (2006)
4. Myers K.M., and Davis M. Mechanisms of fear extinction. Mol. Psychiatry 12 (2007) 120-150
5. McGaugh J.L. Memory - a century of consolidation. Science 287 (2000) 248-251
6. Mason S.T., and Fibiger H. Noradrenaline, fear and extinction. Brain Res. 165 (1979) 47-56
7. McCormick D.A., and Thompson R.F. Locus coeruleus lesions and resistance to extinction of a classically conditioned response: involvement of the neocortex and hippocampus. Brain Res. 245 (1982) 239-249
8. Mueller D., et al. Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J. Neurosci. 28 (2008) 369-375
9. Khoshbouei H., et al. Behavioral reactivity to stress: amplification of stress-induced noradrenergic activation elicits a galanin-mediated anxiolytic effect in central amygdala. Pharmacol. Biochem. Behav. 71 (2002) 407-417
10. Abercrombie E.D., et al. Characterization of hippocampal norepinephrine release as measured by microdialysis perfusion: pharmacological and behavioral studies. Neuroscience 27 (1988) 897-904
11. Aghajanian G.K., and VanderMaelen C.P. alpha 2-adrenoceptor-mediated hyperpolarization of locus coeruleus neurons: intracellular studies in vivo. Science 215 (1982) 1394-1396
12. Becker C., et al. Prevention by 5-HT1A receptor agonists of restraint stress- and yohimbine-induced release of cholecystokinin in the frontal cortex of the freely moving rat. Neuropharmacol. 38 (1999) 525-532
13. Cain C.K., et al. Adrenergic transmission facilitates extinction of conditional fear in mice. Learn Mem. 11 (2004) 179-187
14. Cain C.K., et al. Temporally massed CS presentations generate more fear extinction than spaced presentations. J. Exp. Psychol. Anim. Behav. Process 29 (2003) 323-333
15. Quirk G.J. Learning not to fear, faster. Learn Mem. 11 (2004) 125-126
16. Davis M., et al. Noradrenergic agonists and antagonists: effects on conditioned fear as measured by the potentiated startle paradigm. Psychopharmacology (Berl) 65 (1979) 111-118
17. Holmes A., et al. Evaluation of an anxiety-related phenotype in galanin overexpressing transgenic mice. J. Mol. Neurosci. 18 (2002) 151-165
18. Singewald N., et al. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol. Psychiatry 53 (2003) 275-283
19. Bremner J.D., et al. Noradrenergic mechanisms in stress and anxiety: II. Clinical studies. Synapse 23 (1996) 39-51
20. Foa E.B., and Kozak M.J. Emotional processing of fear: exposure to corrective information. Psychol. Bull. 99 (1986) 20-35
21. Ernst E., and Pittler M.H. Yohimbine for erectile dysfunction: a systematic review and meta-analysis of randomized clinical trials. J. Urol. 159 (1998) 433-436
22. Millstein R.A., and Holmes A. Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci. Biobehav. Rev. 31 (2007) 3-17
23. Camp, M.C. et al. Impaired Pavlovian fear extinction is common across genetic lineages of the 129 inbred mouse strain. Genes Brain. Behav. (in press)
24. Hefner K., et al. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J. Neurosci. 28 (2008) 8074-8085
25. Davis A.R., et al. Yohimbine impairs extinction of cocaine-conditioned place preference in an alpha2-adrenergic receptor independent process. Learn Mem. 15 (2008) 667-676
26. Morris R.W., and Bouton M.E. The effect of yohimbine on the extinction of conditioned fear: a role for context. Behav. Neurosci. 121 (2007) 501-514
27. Bouton M.E., and King D.A. Contextual control of the extinction of conditioned fear: tests for the associative value of the context. J. Exp. Psychol. Anim. Behav. Process 9 (1983) 248-265
28. Woods A.M., and Bouton M.E. D-cycloserine facilitates extinction but does not eliminate renewal of the conditioned emotional response. Behav. Neurosci. 120 (2006) 1159-1162
29. Mueller D., et al. The effects of yohimbine and amphetamine on fear expression and extinction in rats. Psychopharmacology (Berl) 204 (2009) 599-606
30. Bouton M.E. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol. Psychiatry 52 (2002) 976-986
31. Telegdy G., et al. Effects of a new antidepressant drug on active avoidance behavior in rats. Comparative study with tricyclic antidepressants. Arch. Int. Pharmacodyn. Ther. 266 (1983) 50-59
32. Thomas D.R., et al. Pharmacological characterisation of [35S]-GTPgammaS binding to Chinese hamster ovary cell membranes stably expressing cloned human 5-HT1D receptor subtypes. J. Recept. Signal Transduct. Res. 15 (1995) 199-211
33. Millan M.J., et al. Agonist and antagonist actions of yohimbine as compared to fluparoxan at alpha(2)-adrenergic receptors (AR)s, serotonin (5-HT)(1A), 5-HT(1B), 5-HT(1D) and dopamine D(2) and D(3) receptors. Significance for the modulation of frontocortical monoaminergic transmission and depressive states. Synapse 35 (2000) 79-95
34. Newman-Tancredi A., et al. Actions of alpha2 adrenoceptor ligands at alpha2A and 5-HT1A receptors: the antagonist, atipamezole, and the agonist, dexmedetomidine, are highly selective for alpha2A adrenoceptors. Naunyn Schmiedebergs Arch. Pharmacol. 358 (1998) 197-206
35. Winter J.C., and Rabin R.A. Antagonism of the stimulus effects of yohimbine and 8-hydroxydipropylaminotetralin. Pharmacol. Biochem. Behav. 44 (1993) 851-855
36. Llado J., et al. The alpha 2-adrenoceptor antagonist idazoxan is an agonist at 5-HT1A autoreceptors modulating serotonin synthesis in the rat brain in vivo. Neurosci. Lett. 218 (1996) 111-114
37. Herrick-Davis K., et al. Serotonin 5-HT1D receptors in human prefrontal cortex and caudate: interaction with a GTP binding protein. J. Neurochem. 51 (1988) 1906-1912
38. Weinshank R.L., et al. Human serotonin 1D receptor is encoded by a subfamily of two distinct genes: 5-HT1D alpha and 5-HT1D beta. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 3630-3634
39. Scatton B., et al. Antidopaminergic properties of yohimbine. J. Pharmacol. Exp. Ther. 215 (1980) 494-499
40. Waeber C., and Palacios J.M. 5-HT1 receptor binding sites in the guinea pig superior colliculus are predominantly of the 5-HT1D class and are presynaptically located on primary retinal afferents. Brain Res. 528 (1990) 207-211
41. Rodriguez-Romaguera J., et al. Systemic propranolol acts centrally to reduce conditioned fear in rats without impairing extinction. Biol. Psychiatry 65 (2009) 887-892
42. Arthur J.M., et al. Partial agonist properties of rauwolscine and yohimbine for the inhibition of adenylyl cyclase by recombinant human 5-HT1A receptors. Biochem. Pharmacol. 45 (1993) 2337-2341
43. Winter J.C., and Rabin R.A. Yohimbine as a serotonergic agent: evidence from receptor binding and drug discrimination. J. Pharmacol. Exp. Ther. 263 (1992) 682-689
44. Sanger D.J., and Schoemaker H. Discriminative stimulus properties of 8-OH-DPAT: relationship to affinity for 5HT1A receptors. Psychopharmacology (Berl) 108 (1992) 85-92
45. Powell S.B., et al. Yohimbine disrupts prepulse inhibition in rats via action at 5-HT1A receptors, not alpha2-adrenoceptors. Psychopharmacology (Berl) 180 (2005) 491-500
46. Dzung Le A., et al. The role of noradrenaline and 5-hydroxytryptamine in yohimbine-induced increases in alcohol-seeking in rats. Psychopharmacology (Berl) 204 (2009) 477-488
47. Cole J.C., et al. Anxiolytic-like effects of yohimbine in the murine plus-maze: strain independence and evidence against alpha 2-adrenoceptor mediation. Psychopharmacology (Berl) 118 (1995) 425-436
48. De Vry J., et al. Shock-induced ultrasonic vocalization in young adult rats: a model for testing putative anti-anxiety drugs. Eur. J. Pharmacol. 249 (1993) 331-339
49. Wellman C.L., et al. Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J. Neurosci. 27 (2007) 684-691
50. Burghardt N.S., et al. Acute selective serotonin reuptake inhibitors increase conditioned fear expression: blockade with a 5-HT(2C) receptor antagonist. Biol. Psychiatry 62 (2007) 1111-1118
51. Norcross M., et al. Effects of adolescent fluoxetine treatment on fear-, anxiety- or stress-related behaviors in C57BL/6J or BALB/cJ mice. Psychopharmacology (Berl) 200 (2008) 413-424
52. Gobert A., et al. Alpha2-adrenergic receptor blockade markedly potentiates duloxetine- and fluoxetine-induced increases in noradrenaline, dopamine, and serotonin levels in the frontal cortex of freely moving rats. J. Neurochem. 69 (1997) 2616-2619
53. Gobert A., et al. Simultaneous quantification of serotonin, dopamine and noradrenaline levels in single frontal cortex dialysates of freely-moving rats reveals a complex pattern of reciprocal auto- and heteroreceptor-mediated control of release. Neuroscience 84 (1998) 413-429
54. Ponnusamy R., et al. Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice. Learn Mem. 12 (2005) 399-406
55. Nader K., and LeDoux J. The dopaminergic modulation of fear: quinpirole impairs the recall of emotional memories in rats. Behav. Neurosci. 113 (1999) 152-165
56. Powers M.B., et al. Facilitation of fear extinction in phobic participants with a novel cognitive enhancer: a randomized placebo controlled trial of yohimbine augmentation. J. Anxiety Disord. 23 (2009) 350-356
57. Van Der Kolk B.A. The psychobiology and psychopharmacology of PTSD. Hum. Psychopharmacol. (2001) 16
58. Southwick S.M., et al. Yohimbine use in a natural setting: effects on posttraumatic stress disorder. Biol. Psychiatry. 46 (1999) 442-444
59. Charney D.S., et al. Neurobiological mechanisms of panic anxiety: biochemical and behavioral correlates of yohimbine-induced panic attacks. Am. J. Psychiatry. 144 (1987) 1030-1036
60. Foa E.B. Psychosocial therapy for posttraumatic stress disorder. J. Clin. Psychiatry 67 Suppl 2 (2006) 40-45
61. Norton P.J., and Price E.C. A meta-analytic review of adult cognitive-behavioral treatment outcome across the anxiety disorders. J. Nerv. Ment. Dis. 195 (2007) 521-531
62. Davis M., et al. Effects of D-cycloserine on extinction: translation from preclinical to clinical work. Biol. Psychiatry 60 (2006) 369-375
63. Yehuda R., and LeDoux J. Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 56 (2007) 19-32
64. Uher R., and McGuffin P. The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: review and methodological analysis. Mol. Psychiatry 13 (2008) 131-146
65. Hariri A.R., and Holmes A. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn. Sci. 10 (2006) 182-191
66. Caspi A., and Moffitt T.E. Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat. Rev. Neurosci. 7 (2006) 583-590
67. Rau V., et al. Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder. Neurosci. Biobehav. Rev. 29 (2005) 1207-1223
68. Izquierdo A., et al. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J. Neurosci. 26 (2006) 5733-5738
69. Miracle A.D., et al. Chronic stress impairs recall of extinction of conditioned fear. Neurobiol. Learn Mem. 85 (2006) 213-218
70. Muigg P., et al. Impaired extinction of learned fear in rats selectively bred for high anxiety - evidence of altered neuronal processing in prefrontal-amygdala pathways. Eur. J. Neurosci. 28 (2008) 2299-2309