Distinct profiles of anxiety and dysphoria during spontaneous withdrawal from acute morphine exposure

Neuropsychopharmacology

Volumn 34, Issue 10, 2009, Pages 2285-2295

  Rothwell, Patrick E ^a   Thomas, Mark J ^a   Gewirtz, Jonathan C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Acoustic startle; Anxiety; Dysphoria; Morphine; Place conditioning; Withdrawal

Indexed keywords

CHLORDIAZEPOXIDE; DECAHYDRO 6 PHOSPHONOMETHYL 3 ISOQUINOLINECARBOXYLIC ACID; MORPHINE; NALOXONE; OPIATE RECEPTOR; PROPRANOLOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONDITIONING; CONTROLLED STUDY; DYSPHORIA; MALE; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; RECEPTOR OCCUPANCY; REWARD; STARTLE REFLEX; WITHDRAWAL SYNDROME;

ACOUSTIC STIMULATION; ANALYSIS OF VARIANCE; ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; CHLORDIAZEPOXIDE; CONDITIONING, OPERANT; DEPRESSION; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; ISOQUINOLINES; MALE; MORPHINE; NALOXONE; NARCOTIC ANTAGONISTS; NARCOTICS; PROPRANOLOL; RATS; RATS, SPRAGUE-DAWLEY; STARTLE REACTION; SUBSTANCE WITHDRAWAL SYNDROME; TIME FACTORS;

EID: 68949177132     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2009.56     Document Type: Article

References (91)

1. American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders : DSM-IV-TR, 4th edn. American Psychiatric Association: Washington, DC, xxxvii, 943 p.pp.
2. Araki H, Kawakami KY, Jin C, Suemaru K, Kitamura Y, Nagata M et al (2004). Nicotine attenuates place aversion induced by naloxone in single-dose, morphine-treated rats. Psychopharmacology (Berl) 171: 398-404.
3. Babbini M, Davis WM (1972). Time-dose relationships for locomotor activity effects of morphine after acute or repeated treatment. Br J Pharmacol 46: 213-224.
4. Baker TB, Piper ME, McCarthy DE, Majeskie MR, Fiore MC (2004). Addiction motivation reformulated: an affective processing model of negative reinforcement. Psychol Rev 111: 33-51.
5. Bardo MT, Bevins RA (2000). Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology (Berl) 153: 31-43.
6. Barjavel MJ, Scherrmann JM, Bhargava HN (1995). Relationship between morphine analgesia and cortical extracellular fluid levels of morphine and its metabolites in the rat: a microdialysis study. Br J Pharmacol 116: 3205-3210.
7. Barr AM, Markou A, Phillips AG (2002). A 'crash' course on psychostimulant withdrawal as a model of depression. Trends Pharmacol Sci 23: 475-482.
8. Bechara A, Nader K, van der Kooy D (1995). Neurobiology of withdrawal motivation: evidence for two separate aversive effects produced in morphine-naive vs morphine-dependent rats by both naloxone and spontaneous withdrawal. Behav Neurosci 109: 91-105.
9. Bilsky EJ, Inturrisi CE, Sadee W, Hruby VJ, Porreca F (1996). Competitive and non-competitive NMDA antagonists block the development of antinociceptive tolerance to morphine, but not to selective mu or delta opioid agonists in mice. Pain 68: 229-237.
10. Bosch OJ, Nair HP, Ahern TH, Neumann ID, Young LJ (2008). The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacology 34: 1406-1415.
11. Breiter HC, Gollub RL, Weisskoff RM, Kennedy DN, Makris N, Berke JD et al (1997). Acute effects of cocaine on human brain activity and emotion. Neuron 19: 591-611.
12. Cabral A, Ruggiero RN, Nobre MJ, Brandao ML, Castilho VM (2009). GABA and opioid mechanisms of the central amygdala underlie the withdrawal-potentiated startle from acute morphine. Prog Neuropsychopharmacol Biol Psychiatry 33: 334-344.
13. Carboni E, Silvagni A, Rolando MT, Di Chiara G (2000). Stimulation of in vivo dopamine transmission in the bed nucleus of stria terminalis by reinforcing drugs. J Neurosci 20: RC102.
14. Carlezon Jr WA (2003). Place conditioning to study drug reward and aversion. Methods Mol Med 84: 243-249.
15. Carlezon Jr WA, Chartoff EH (2007). Intracranial self-stimulation (ICSS) in rodents to study the neurobiology of motivation. Nat Protoc 2: 2987-2995.
16. Cole BJ, Koob GF (1988). Propranolol antagonizes the enhanced conditioned fear produced by corticotropin releasing factor. J Pharmacol Exp Ther 247: 902-910.
17. Criner SH, Liu J, Schulteis G (2007). Rapid neuroadaptation in the nucleus accumbens and bed nucleus of the stria terminalis mediates suppression of operant responding during withdrawal from acute opioid dependence. Neuroscience 144: 1436-1446.
18. Cunningham CL, Gremel CM, Groblewski PA (2006). Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1: 1662-1670.
19. de Jongh R, Groenink L, van Der Gugten J, Olivier B (2002). The light-enhanced startle paradigm as a putative animal model for anxiety: effects of chlordiazepoxide, flesinoxan and fluvoxamine. Psychopharmacology (Berl) 159: 176-180.
20. Di Chiara G, Imperato A (1988). Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85: 5274-5278.
21. Diana M, Pistis M, Muntoni A, Gessa G (1995). Profound decrease of mesolimbic dopaminergic neuronal activity in morphine withdrawn rats. J Pharmacol Exp Ther 272: 781-785.
22. Dichter GS, Tomarken AJ (2008). The chronometry of affective startle modulation in unipolar depression. J Abnorm Psychol 117: 1-15.
23. Dole VP, Nyswander ME, Kreek MJ (1966). Narcotic blockade. Arch Intern Med 118: 304-309.
24. Eisenberg RM (1982). Further studies on the acute dependence produced by morphine in opiate naive rats. Life Sci 31: 1531-1540.
25. Ettenberg A, Bernardi RE (2007). Effects of buspirone on the immediate positive and delayed negative properties of intravenous cocaine as measured in the conditioned place preference test. Pharmacol Biochem Behav 87: 171-178.
26. Fendt M, Mucha RF (2001). Anxiogenic-like effects of opiate withdrawal seen in the fear-potentiated startle test, an interdisciplinary probe for drug-related motivational states. Psychopharmacology (Berl) 155: 242-250.
27. Fenu S, Spina L, Rivas E, Longoni R, Di Chiara G (2006). Morphine-conditioned single-trial place preference: role of nucleus accumbens shell dopamine receptors in acquisition, but not expression. Psychopharmacology (Berl) 187: 143-153.
28. Forbes EE, Miller A, Cohn JF, Fox NA, Kovacs M (2005). Affect-modulated startle in adults with childhood-onset depression: relations to bipolar course and number of lifetime depressive episodes. Psychiatry Res 134: 11-25.
29. Gellert VF, Sparber SB (1977). A comparison of the effects of naloxone upon body weight loss and suppression of fixed-ratio operant behavior in morphine-dependent rats. J Pharmacol Exp Ther 201: 44-54.
30. Goldberg D (2008). Towards DSM-V: the relationship between generalized anxiety disorder and major depressive episode. Psychol Med 38: 1671-1675.
31. Goldstein A, Naidu A (1989). Multiple opioid receptors: ligand selectivity profiles and binding site signatures. Mol Pharmacol 36: 265-272.
32. Haertzen CA, Hooks Jr NT (1969). Changes in personality and subjective experience associated with the chronic administration and withdrawal of opiates. J Nerv Ment Dis 148: 606-614.
33. Harris AC, Atkinson DM, Aase DM, Gewirtz JC (2006). Double dissociation in the neural substrates of acute opiate dependence as measured by withdrawal-potentiated startle. Neuroscience 139: 1201-1210.
34. Harris AC, Gewirtz JC (2004a). Elevated startle during withdrawal from acute morphine: a model of opiate withdrawal and anxiety. Psychopharmacology (Berl) 171: 140-147.
35. Harris AC, Gewirtz JC (2005). Acute opioid dependence: characterizing the early adaptations underlying drug withdrawal. Psychopharmacology (Berl) 178: 353-366.
36. Harris AC, Hanes SL, Gewirtz JC (2004b). Potentiated startle and hyperalgesia during withdrawal from acute morphine: effects of multiple opiate exposures. Psychopharmacology (Berl) 176: 266-273.
37. Harris AC, Rothwell PE, Gewirtz JC (2008). Effects of the NMDA receptor antagonist memantine on the expression and development of acute opiate dependence as assessed by withdrawal-potentiated startle and hyperalgesia. Psychopharmacology (Berl) 196: 649-660.
38. Harris GC, Aston-Jones G (1993a). Beta-adrenergic antagonists attenuate somatic and aversive signs of opiate withdrawal. Neuropsychopharmacology 9: 303-311.
39. Harris GC, Aston-Jones G (1993b). Beta-adrenergic antagonists attenuate withdrawal anxiety in cocaine- and morphine-dependent rats. Psychopharmacology (Berl) 113: 131-136.
40. Heishman SJ, Stitzer ML, Bigelow GE, Liebson IA (1989). Acute opioid physical dependence in humans: effect of varying the morphine-naloxone interval. I. J Pharmacol Exp Ther 250: 485-491.
41. Hipps PP, Eveland MR, Meyer ER, Sherman WR, Cicero TJ (1976). Mass fragmentography of morphine: relationship between brain levels and analgesic activity. J Pharmacol Exp Ther 196: 642-648.
42. Houshyar H, Gomez F, Manalo S, Bhargava A, Dallman MF (2003). Intermittent morphine administration induces dependence and is a chronic stressor in rats. Neuropsychopharmacology 28: 1960-1972.
43. Houshyar H, Manalo S, Dallman MF (2004). Time-dependent alterations in mRNA expression of brain neuropeptides regulating energy balance and hypothalamo-pituitary-adrenal activity after withdrawal from intermittent morphine treatment. J Neurosci 24: 9414-9424.
44. Hurd YL, McGregor A, Ponten M (1997). In vivo amygdala dopamine levels modulate cocaine self-administration behaviour in the rat: D1 dopamine receptor involvement. Eur J Neurosci 9: 2541-2548.
45. Jones KL, Zhu H, Jenab S, Du T, Inturrisi CE, Barr GA (2002). Attenuation of acute morphine withdrawal in the neonatal rat by the competitive NMDA receptor antagonist LY235959. Neuropsychopharmacology 26: 301-310.
46. Kalinichev M, Holtzman SG (2003). Changes in urination/defecation, auditory startle response, and startle-induced ultrasonic vocalizations in rats undergoing morphine withdrawal: similarities and differences between acute and chronic dependence. J Pharmacol Exp Ther 304: 603-609.
47. Kawasaki Y, Jin C, Suemaru K, Kawasaki H, Shibata K, Choshi T et al (2005). Effect of glutamate receptor antagonists on place aversion induced by naloxone in single-dose morphine-treated rats. Br J Pharmacol 145: 751-757.
48. Keppel G, Wickens TD (2004). Design and Analysis : A Researcher's Handbook. Pearson Prentice Hall: Upper Saddle River, NJ. xii, 611 p.pp.
49. Kessler RC, Gruber M, Hettema JM, Hwang I, Sampson N, Yonkers KA (2008). Co-morbid major depression and generalized anxiety disorders in the National Comorbidity Survey follow-up. Psychol Med 38: 365-374.
50. Kirby KC, Stitzer ML (1993). Opioid physical dependence development in humans: effect of time between agonist pretreatments. Psychopharmacology (Berl) 112: 511-517.
51. Knoll AT, Meloni EG, Thomas JB, Carroll FI, Carlezon Jr WA (2007). Anxiolytic-like effects of kappa-opioid receptor antagonists in models of unlearned and learned fear in rats. J Pharmacol Exp Ther 323: 838-845.
52. Koob GF, Le Moal M (2008). Addiction and the brain antireward system. Annu Rev Psychol 59: 29-53.
53. Krueger RF (1999). The structure of common mental disorders. Arch Gen Psychiatry 56: 921-926.
54. Land BB, Bruchas MR, Lemos JC, Chavkin C (2008a). Distinct roles for CRF receptor subtypes 1 and 2 in producing dynorphin/kappa opioid receptor-dependent anxiety and conditioned place aversion. Abstr Soc Neurosci 34: 187.1.
55. Land BB, Bruchas MR, Lemos JC, Xu M, Melief EJ, Chavkin C (2008b). The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci 28: 407-414.
56. Lang PJ, Davis M, Ohman A (2000). Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 61: 137-159.
57. Lang PJ, McTeague LM (2009). The anxiety disorder spectrum: fear imagery, physiological reactivity, and differential diagnosis. Anxiety Stress Coping 22: 5-25.
58. Laulin JP, Larcher A, Celerier E, Le Moal M, Simonnet G (1998). Long-lasting increased pain sensitivity in rat following exposure to heroin for the first time. Eur J Neurosci 10: 782-785.
59. Le Guen S, Gestreau C, Besson JM (2003). Morphine withdrawal precipitated by specific mu, delta or kappa opioid receptor antagonists: a c-Fos protein study in the rat central nervous system. Eur J Neurosci 17: 2425-2437.
60. Liu J, Schulteis G (2004). Brain reward deficits accompany naloxone-precipitated withdrawal from acute opioid dependence. Pharmacol Biochem Behav 79: 101-108.
61. Maldonado R, Negus S, Koob GF (1992). Precipitation of morphine withdrawal syndrome in rats by administration of mu-, delta- and kappa-selective opioid antagonists. Neuropharmacology 31: 1231-1241.
62. Mansbach RS, Gold LH, Harris LS (1992). The acoustic startle response as a measure of behavioral dependence in rats. Psychopharmacology (Berl) 108: 40-46.
63. Mendez IA, Trujillo KA (2008). NMDA receptor antagonists inhibit opiate antinociceptive tolerance and locomotor sensitization in rats. Psychopharmacology (Berl) 196: 497-509.
64. Morse AC, Schulteis G, Holloway FA, Koob GF (2000). Conditioned place aversion to the 'hangover' phase of acute ethanol administration in the rat. Alcohol 22: 19-24.
65. Motta V, Penha K, Brandao ML (1995). Effects of microinjections of mu and kappa receptor agonists into the dorsal periaqueductal gray of rats submitted to the plus maze test. Psychopharmacology (Berl) 120: 470-474.
66. Nestler EJ, Carlezon Jr WA (2006). The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59: 1151-1159.
67. Nobre MJ, Ribeiro dos Santos N, Aguiar MS, Brandao ML (2000). Blockade of mu- and activation of kappa-opioid receptors in the dorsal periaqueductal gray matter produce defensive behavior in rats tested in the elevated plus-maze. Eur J Pharmacol 404: 145-151.
68. Pain L, Oberling P, Mainsongeon M, Moulinoux JP, Simonnet G (2008). Delayed aversive effects of high-dose fentanyl. Prevention by a polyamine-deficient diet. Behav Brain Res 190: 119-123.
69. Parker LA, Joshi A (1998). Naloxone-precipitated morphine withdrawal induced place aversions: effect of naloxone at 24 h postmorphine. Pharmacol Biochem Behav 61: 331-333.
70. Pfeiffer A, Brantl V, Herz A, Emrich HM (1986). Psychotomimesis mediated by kappa opiate receptors. Science 233: 774-776.
71. Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon Jr WA (2001). Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 21: 7397-7403.
72. Pothos E, Rada P, Mark GP, Hoebel BG (1991). Dopamine microdialysis in the nucleus accumbens during acute and chronic morphine, naloxone-precipitated withdrawal and clonidine treatment. Brain Res 566: 348-350.
73. Rasmussen K (1995). The role of the locus coeruleus and N-methyl-D-aspartic acid (NMDA) and AMPA receptors in opiate withdrawal. Neuropsychopharmacology 13: 295-300.
74. Risbrough VB, Brodkin JD, Geyer MA (2003). GABA-A and 5-HT1A receptor agonists block expression of fear-potentiated startle in mice. Neuropsychopharmacology 28: 654-663.
75. Rodriguez-Romaguera J, Sotres-Bayon F, Mueller D, Quirk GJ (2009). Systemic propranolol acts centrally to reduce conditioned fear in rats without impairing extinction. Biol Psychiatry 65: 887-892.
76. Rossetti ZL, Hmaidan Y, Gessa GL (1992). Marked inhibition of mesolimbic dopamine release: a common feature of ethanol, morphine, cocaine and amphetamine abstinence in rats. Eur J Pharmacol 221: 227-234.
77. Sahuque LL, Kullberg EF, McGeehan AJ, Kinder JR, Hicks MP, Blanton MG et al (2006). Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: role of CRF receptor subtypes. Psychopharmacology (Berl) 186: 122-132.
78. Sante AB, Nobre MJ, Brandao ML (2000). Place aversion induced by blockade of mu or activation of kappa opioid receptors in the dorsal periaqueductal gray matter. Behav Pharmacol 11: 583-589.
79. Schulteis G, Markou A, Gold LH, Stinus L, Koob GF (1994). Relative sensitivity to naloxone of multiple indices of opiate withdrawal: a quantitative dose-response analysis. J Pharmacol Exp Ther 271: 1391-1398.
80. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003). The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168: 3-20.
81. Shippenberg TS, Zapata A, Chefer VI (2007). Dynorphin and the pathophysiology of drug addiction. Pharmacol Ther 116: 306-321.
82. Spanagel R, Almeida OF, Bartl C, Shippenberg TS (1994). Endogenous kappa-opioid systems in opiate withdrawal: role in aversion and accompanying changes in mesolimbic dopamine release. Psychopharmacology (Berl) 115: 121-127.
83. Sweitzer SM, Allen CP, Zissen MH, Kendig JJ (2004). Mechanical allodynia and thermal hyperalgesia upon acute opioid withdrawal in the neonatal rat. Pain 110: 269-280.
84. Van Dyke C, Byck R (1982). Cocaine. Sci Am 246: 128-141.
85. Vargas-Perez H, Ting AKRA, Heinmiller A, Sturgess JE, van der Kooy D (2007). A test of the opponent-process theory of motivation using lesions that selectively block morphine reward. Eur J Neurosci 25: 3713-3718.
86. Walker DL, Davis M (2002a). Light-enhanced startle: further pharmacological and behavioral characterization. Psychopharmacology (Berl) 159: 304-310.
87. Walker DL, Davis M (2002b). Quantifying fear potentiated startle using absolute vs proportional increase scoring methods: implications for the neurocircuitry of fear and anxiety. Psychopharmacology (Berl) 164: 318-328.
88. Walker DL, Toufexis DJ, Davis M (2003). Role of the bed nucleus of the stria terminalis vs the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463: 199-216.
89. Wallace DL, Han MH, Graham DL, Green TA, Vialou V, Iniguez SD et al (2009). CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12: 200-209.
90. White DA, Hwang ML, Holtzman SG (2005). Naltrexone-induced conditioned place aversion following a single dose of morphine in the rat. Pharmacol Biochem Behav 81: 451-458.
91. Yamada H, Shimoyama N, Sora I, Uhl GR, Fukuda Y, Moriya H et al (2006). Morphine can produce analgesia via spinal kappa opioid receptors in the absence of mu opioid receptors. Brain Res 1083: 61-69.