Development of mechanical hypersensitivity in rats during heroin and ethanol dependence: Alleviation by CRF 1 receptor antagonism

Neuropharmacology

Volumn 62, Issue 2, 2012, Pages 1142-1151

  Edwards, Scott ^a   Vendruscolo, Leandro F ^a   Schlosburg, Joel E ^a   Misra, Kaushik K ^a   Wee, Sunmee ^a   Park, Paula E ^a   Schulteis, Gery ^b,c   Koob, George F ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c University of California   (United States)

Author keywords

Addiction; Cocaine; Corticotropin releasing factor; Ethanol; Heroin; Hyperalgesia

Indexed keywords

ALCOHOL; COCAINE; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; DIAMORPHINE; N,N BIS(2 METHOXYETHYL) 3 (4 METHOXY 2 METHYPHENYL) 2,5 DIMETHYLPYRAZOLO[1,5 A]PYRIMIDIN 7 AMINE; UNCLASSIFIED DRUG;

ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COCAINE DEPENDENCE; CONTROLLED STUDY; CORTICOTROPIN RELEASE; DRUG SENSITIVITY; HEROIN DEPENDENCE; HYPERALGESIA; LONG TERM EXPOSURE; MALE; MECHANICAL HYPERSENSITIVITY; MECHANICAL STIMULATION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; WITHDRAWAL SYNDROME;

ALCOHOLISM; ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; HEROIN; HEROIN DEPENDENCE; HYPERALGESIA; MALE; PAIN PERCEPTION; PAIN THRESHOLD; PHYSICAL STIMULATION; PYRIMIDINES; RATS; RATS, WISTAR; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; REWARD; SELF ADMINISTRATION;

EID: 84855958428     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.11.006     Document Type: Article

References (112)

1. S.H. Ahmed, and G.F. Koob Transition from moderate to excessive drug intake: change in hedonic set point Science 282 1998 298 300
2. S.H. Ahmed, J.R. Walker, and G.F. Koob Persistent increase in the motivation to take heroin in rats with a history of drug escalation Neuropsychopharmacology 22 2000 413 421
3. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders fourth ed. 2000 American Psychiatric Press Washington, DC, USA
4. N. Altier, and J. Stewart The role of dopamine in the nucleus accumbens in analgesia Life Sci. 65 1999 2269 2287
5. M.S. Angst, and J.D. Clark Opioid-induced hyperalgesia: a qualitative systematic review Anesthesiology 104 2006 570 587
6. M. Barrot When chronic pain can suppress the opioid kick: new insights from preclinical research Anesthesiology 114 2011 493 494
7. M. Barrot, J.D. Olivier, L.I. Perrotti, R.J. DiLeone, O. Berton, A.J. Eisch, S. Impey, D.R. Storm, R.L. Neve, J.C. Yin, V. Zachariou, and E.J. Nestler CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli Proc. Natl. Acad. Sci. U S A 99 2002 11435 11440
8. J.B. Bederson, H.L. Fields, and N.M. Barbaro Hyperalgesia during naloxone-precipitated withdrawal from morphine is associated with increased on-cell activity in the rostral ventromedial medulla Somatosens Mot Res. 7 1990 185 203
9. J.F. Bernard, G.F. Huang, and J.M. Besson Effect of noxious somesthetic stimulation on the activity of neurons of the nucleus centralis of the amygdala Brain Res. 523 1990 347 350
10. B. Boutrel A neuropeptide-centric view of psychostimulant addiction Br. J. Pharmacol. 154 2008 343 357
11. P.L. Brennan, K.K. Schutte, and R.H. Moos Pain and use of alcohol to manage pain: prevalence and 3-year outcomes among older problem and non-problem drinkers Addiction 100 2005 777 786
12. Y. Carrasquillo, and R.W.T. Gereau Activation of the extracellular signal-regulated kinase in the amygdala modulates pain perception J. Neurosci. 27 2007 1543 1551
13. E. Celerier, J.P. Laulin, J.B. Corcuff, M. Le Moal, and G. Simonnet Progressive enhancement of delayed hyperalgesia induced by repeated heroin administration: a sensitization process J. Neurosci. 21 2001 4074 4080
14. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J. Neurosci. Methods 53 1994 55 63
15. I. Diamond, and R.O. Messing Neurologic effects of alcoholism West J. Med. 161 1994 279 287
16. O.A. Dina, J. Barletta, X. Chen, A. Mutero, A. Martin, R.O. Messing, and J.D. Levine Key role for the epsilon isoform of protein kinase C in painful alcoholic neuropathy in the rat J. Neurosci. 20 2000 8614 8619
17. O.A. Dina, R.W. Gear, R.O. Messing, and J.D. Levine Severity of alcohol-induced painful peripheral neuropathy in female rats: role of estrogen and protein kinase (A and Cepsilon) Neuroscience 145 2007 350 356
18. O.A. Dina, S.G. Khasar, N. Alessandri-Haber, P.G. Green, R.O. Messing, and J.D. Levine Alcohol-induced stress in painful alcoholic neuropathy Eur. J. Neurosci. 27 2008 83 92
19. O.A. Dina, R.O. Messing, and J.D. Levine Ethanol withdrawal induces hyperalgesia mediated by PKCepsilon Eur. J. Neurosci. 24 2006 197 204
20. W.J. Dixon Efficient analysis of experimental observations Annu. Rev. Pharmacol. Toxicol. 20 1980 441 462
21. S. Edwards, D.L. Graham, K.N. Whisler, and D.W. Self Phosphorylation of GluR1, ERK, and CREB during spontaneous withdrawal from chronic heroin self-administration Synapse 63 2009 224 235
22. S. Edwards, M. Guerrero, O.M. Ghoneim, E. Roberts, and G.F. Koob Evidence that vasopressin V(1b) receptors mediate the transition to excessive drinking in ethanol-dependent rats Addict. Biol. 2011
23. S. Edwards, and G.F. Koob Neurobiology of dysregulated motivational systems in drug addiction Future Neurol. 5 2010 393 401
24. I. Elman, J.K. Zubieta, and D. Borsook The missing p in psychiatric training: why it is important to teach pain to psychiatrists Arch. Gen. Psychiatry 68 2011 12 20
25. A. Ettenberg Opponent process properties of self-administered cocaine Neurosci. Biobehav. Rev. 27 2004 721 728
26. E.E. Ewan, and T.J. Martin Opioid facilitation of rewarding electrical brain stimulation is suppressed in rats with neuropathic pain Anesthesiology 114 2011 624 632
27. H.L. Fields The doctor's dilemma: opiate analgesics and chronic pain Neuron 69 2011 591 594
28. D.A. Fishbain, B. Cole, J. Lewis, H.L. Rosomoff, and R.S. Rosomoff What percentage of chronic nonmalignant pain patients exposed to chronic opioid analgesic therapy develop abuse/addiction and/or aberrant drug-related behaviors? A structured evidence-based review Pain Med. 9 2008 444 459
29. Y. Fu, J. Han, T. Ishola, M. Scerbo, H. Adwanikar, C. Ramsey, and V. Neugebauer PKA and ERK, but not PKC, in the amygdala contribute to pain-related synaptic plasticity and behavior Mol. Pain 4 2008 26
30. Y. Fu, and V. Neugebauer Differential mechanisms of CRF1 and CRF2 receptor functions in the amygdala in pain-related synaptic facilitation and behavior J. Neurosci. 28 2008 3861 3876
31. C.K. Funk, L.E. O'Dell, E.F. Crawford, and G.F. Koob Corticotropin- releasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanol-dependent rats J. Neurosci. 26 2006 11324 11332
32. C.K. Funk, E.P. Zorrilla, M.J. Lee, K.C. Rice, and G.F. Koob Corticotropin-releasing factor 1 antagonists selectively reduce ethanol self-administration in ethanol-dependent rats Biol. Psychiatry 61 2007 78 86
33. R.W. Gear, and J.D. Levine Antinociception produced by an ascending spino-supraspinal pathway J. Neurosci. 15 1995 3154 3161
34. C. Gianoulakis Endogenous opioids and addiction to alcohol and other drugs of abuse Curr. Top. Med. Chem. 9 2009 999 1015
35. N.W. Gilpin, and G.F. Koob Neurobiology of alcohol dependence: focus on motivational mechanisms Alcohol Res. Health 31 2008 185 195
36. N.W. Gilpin, H.N. Richardson, M. Cole, and G.F. Koob Vapor inhalation of alcohol in rats Curr. Protoc. Neurosci. 2008 29 (Chapter 9, Unit 9)
37. T.N. Greenwell, C.K. Funk, P. Cottone, H.N. Richardson, S.A. Chen, K.C. Rice, E.P. Zorrilla, and G.F. Koob Corticotropin-releasing factor-1 receptor antagonists decrease heroin self-administration in long- but not short-access rats Addict. Biol. 14 2009 130 143
38. H.B. Gutstein The effects of pain on opioid tolerance: how do we resolve the controversy? Pharmacol. Rev. 48 1996 403 407 discussion 409-411
39. M. Heilig, A. Thorsell, W.H. Sommer, A.C. Hansson, V.A. Ramchandani, D.T. George, D. Hommer, and C.S. Barr Translating the neuroscience of alcoholism into clinical treatments: from blocking the buzz to curing the blues Neurosci. Biobehav. Rev. 35 2010 334 344
40. S.C. Heinrichs, F. Menzaghi, G. Schulteis, G.F. Koob, and L. Stinus Suppression of corticotropin-releasing factor in the amygdala attenuates aversive consequences of morphine withdrawal Behav. Pharmacol. 6 1995 74 80
41. A. Herz Endogenous opioid systems and alcohol addiction Psychopharmacology (Berl) 129 1997 99 111
42. M.M. Huang, D.H. Overstreet, D.J. Knapp, R. Angel, T.A. Wills, M. Navarro, J. Rivier, W. Vale, and G.R. Breese Corticotropin-releasing factor (CRF) sensitization of ethanol withdrawal-induced anxiety-like behavior is brain site specific and mediated by CRF-1 receptors: relation to stress-induced sensitization J. Pharmacol. Exp. Ther. 332 2010 298 307
43. T. Imaki, J.L. Nahan, C. Rivier, P.E. Sawchenko, and W. Vale Differential regulation of corticotropin-releasing factor mRNA in rat brain regions by glucocorticoids and stress J. Neurosci. 11 1991 585 599
44. G. Ji, Y. Fu, K.A. Ruppert, and V. Neugebauer Pain-related anxiety-like behavior requires CRF1 receptors in the amygdala Mol. Pain 3 2007 13
45. G. Ji, and V. Neugebauer Differential effects of CRF1 and CRF2 receptor antagonists on pain-related sensitization of neurons in the central nucleus of the amygdala J. Neurophysiol. 97 2007 3893 3904
46. G. Ji, and V. Neugebauer Pro- and anti-nociceptive effects of corticotropin-releasing factor (CRF) in central amygdala neurons are mediated through different receptors J. Neurophysiol. 99 2008 1201 1212
47. T. Jochum, M.K. Boettger, C. Burkhardt, G. Juckel, and K.J. Bar Increased pain sensitivity in alcohol withdrawal syndrome Eur. J. Pain 14 2010 713 718
48. C.B. Johannes, T.K. Le, X. Zhou, J.A. Johnston, and R.H. Dworkin The prevalence of chronic pain in United States adults: results of an internet-based survey J. Pain 11 2010 1230 1239
49. H. Kaplan, and H.L. Fields Hyperalgesia during acute opioid abstinence: evidence for a nociceptive facilitating function of the rostral ventromedial medulla J. Neurosci. 11 1991 1433 1439
50. P.J. Kenny, S.A. Chen, O. Kitamura, A. Markou, and G.F. Koob Conditioned withdrawal drives heroin consumption and decreases reward sensitivity J. Neurosci. 26 2006 5894 5900
51. T. King, L. Vera-Portocarrero, T. Gutierrez, T.W. Vanderah, G. Dussor, J. Lai, H.L. Fields, and F. Porreca Unmasking the tonic-aversive state in neuropathic pain Nat. Neurosci. 12 2009 1364 1366
52. G.F. Koob A role for brain stress systems in addiction Neuron 59 2008 11 34
53. G.F. Koob, and F.E. Bloom Cellular and molecular mechanisms of drug dependence Science 242 1988 715 723
54. G.F. Koob, G. Kenneth Lloyd, and B.J. Mason Development of pharmacotherapies for drug addiction: a Rosetta stone approach Nat. Rev. Drug Discov. 8 2009 500 515
55. G.F. Koob, and M. Le Moal Drug abuse: hedonic homeostatic dysregulation Science 278 1997 52 58
56. G.F. Koob, and M. Le Moal Addiction and the brain antireward system Annu. Rev. Psychol. 59 2008 29 53
57. G.F. Koob, A.J. Roberts, B.L. Kieffer, C.J. Heyser, S.N. Katner, R. Ciccocioppo, and F. Weiss Animal models of motivation for drinking in rodents with a focus on opioid receptor neuropharmacology Recent Dev. Alcohol 16 2003 263 281
58. M.J. Kreek Cocaine, dopamine and the endogenous opioid system J. Addict. Dis. 15 1996 73 96
59. D. Labuz, S. Berger, S.A. Mousa, C. Zollner, H.L. Rittner, M.A. Shaqura, T. Segovia-Silvestre, B. Przewlocka, C. Stein, and H. Machelska Peripheral antinociceptive effects of exogenous and immune cell-derived endomorphins in prolonged inflammatory pain J. Neurosci. 26 2006 4350 4358
60. D. Labuz, A. Schreiter, Y. Schmidt, A. Brack, and H. Machelska T lymphocytes containing beta-endorphin ameliorate mechanical hypersensitivity following nerve injury Brain Behav. Immun. 24 2010 1045 1053
61. W.R. Lariviere, P. Fiorenzani, I. Ceccarelli, C. Massafra, G. Sorda, C. Di Canio, and A.M. Aloisi Central CRH administration changes formalin pain responses in male and female rats Brain Res. 1383 2011 128 134
62. W.R. Lariviere, and R. Melzack The role of corticotropin-releasing factor in pain and analgesia Pain 84 2000 1 12
63. J.P. Laulin, A. Larcher, E. Celerier, M. Le Moal, and G. Simonnet Long-lasting increased pain sensitivity in rat following exposure to heroin for the first time Eur. J. Neurosci. 10 1998 782 785
64. M. Lenoir, and S.H. Ahmed Heroin-induced reinstatement is specific to compulsive heroin use and dissociable from heroin reward and sensitization Neuropsychopharmacology 32 2007 616 624
65. M.L. Logrip, G.F. Koob, and E.P. Zorrilla Role of corticotropin-releasing factor in drug addiction: potential for pharmacological intervention CNS Drugs 25 2011 271 287
66. S. Makino, P.W. Gold, and J. Schulkin Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus Brain Res. 640 1994 105 112
67. T.J. Martin, N.L. Buechler, S.A. Kim, E.E. Ewan, R. Xiao, and S.R. Childers Involvement of the lateral amygdala in the antiallodynic and reinforcing effects of heroin in rats after peripheral nerve injury Anesthesiology 114 2011 633 642
68. T.J. Martin, S.A. Kim, N.L. Buechler, F. Porreca, and J.C. Eisenach Opioid self- administration in the nerve-injured rat: relevance of antiallodynic effects to drug consumption and effects of intrathecal analgesics Anesthesiology 106 2007 312 322
69. J.C. Maxwell The prescription drug epidemic in the United States: a perfect storm Drug Alcohol Rev. 30 2011 264 270
70. C.A. McClung The molecular mechanisms of morphine addiction Rev. Neurosci. 17 2006 393 402
71. G.P. McNally, and H. Akil Role of corticotropin-releasing hormone in the amygdala and bed nucleus of the stria terminalis in the behavioral, pain modulatory, and endocrine consequences of opiate withdrawal Neuroscience 112 2002 605 617
72. E. Merlo Pich, M. Lorang, M. Yeganeh, F. Rodriguez de Fonseca, J. Raber, G.F. Koob, and F. Weiss Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis J. Neurosci. 15 1995 5439 5447
73. N.S. Miller, and M.S. Gold Opiate prescription medication dependence and pain perceptions J. Addict. Dis. 26 Suppl 1 2007 65 71
74. V. Modesto-Lowe, and E.M. Fritz The opioidergic-alcohol link: implications for treatment CNS Drugs 19 2005 693 707
75. S.A. Mousa, C.P. Bopaiah, J.F. Richter, R.S. Yamdeu, and M. Schafer Inhibition of inflammatory pain by CRF at peripheral, spinal and supraspinal sites: involvement of areas coexpressing CRF receptors and opioid peptides Neuropsychopharmacology 32 2007 2530 2542
76. S.A. Mousa, C.P. Bopaiah, C. Stein, and M. Schafer Involvement of corticotropin-releasing hormone receptor subtypes 1 and 2 in peripheral opioid-mediated inhibition of inflammatory pain Pain 106 2003 297 307
77. E.J. Nestler, and G.K. Aghajanian Molecular and cellular basis of addiction Science 278 1997 58 63
78. V. Neugebauer, W. Li, G.C. Bird, and J.S. Han The amygdala and persistent pain Neuroscientist 10 2004 221 234
79. M.F. Olive, H.N. Koenig, M.A. Nannini, and C.W. Hodge Elevated extracellular CRF levels in the bed nucleus of the stria terminalis during ethanol withdrawal and reduction by subsequent ethanol intake Pharmacol. Biochem. Behav. 72 2002 213 220
80. L. Orio, S. Edwards, O. George, L.H. Parsons, and G.F. Koob A role for the endocannabinoid system in the increased motivation for cocaine in extended-access conditions J. Neurosci. 29 2009 4846 4857
81. M.H. Ossipov, J. Lai, T. King, T.W. Vanderah, T.P. Malan Jr., V.J. Hruby, and F. Porreca Antinociceptive and nociceptive actions of opioids J. Neurobiol. 61 2004 126 148
82. F.A. Pamplona, L.F. Vendruscolo, and R.N. Takahashi Increased sensitivity to cocaine-induced analgesia in Spontaneously Hypertensive Rats (SHR) Behav. Brain Funct. 3 2007 9
83. Z.Y. Ren, J. Shi, D.H. Epstein, J. Wang, and L. Lu Abnormal pain response in pain-sensitive opiate addicts after prolonged abstinence predicts increased drug craving Psychopharmacology (Berl) 204 2009 423 429
84. H.N. Richardson, Y. Zhao, E.M. Fekete, C.K. Funk, P. Wirsching, K.D. Janda, E.P. Zorrilla, and G.F. Koob MPZP: a novel small molecule corticotropin-releasing factor type 1 receptor (CRF1) antagonist Pharmacol. Biochem. Behav. 88 2008 497 510
85. J.L. Riley 3rd, and C. King Self-report of alcohol use for pain in a multi-ethnic community sample J. Pain 10 2009 944 952
86. D.G. Ririe, and J.C. Eisenach Age-dependent responses to nerve injury-induced mechanical allodynia Anesthesiology 104 2006 344 350
87. A.J. Roberts, C.J. Heyser, M. Cole, P. Griffin, and G.F. Koob Excessive ethanol drinking following a history of dependence: animal model of allostasis Neuropsychopharmacology 22 2000 581 594
88. J. Rogers, S.G. Wiener, and F.E. Bloom Long-term ethanol administration methods for rats: advantages of inhalation over intubation or liquid diets Behav. Neural Biol. 27 1979 466 486
89. I. Roth-Deri, A. Zangen, M. Aleli, R.G. Goelman, G. Pelled, R. Nakash, I. Gispan-Herman, T. Green, Y. Shaham, and G. Yadid Effect of experimenter- delivered and self-administered cocaine on extracellular beta-endorphin levels in the nucleus accumbens J. Neurochem. 84 2003 930 938
90. R. Salimov, N. Salimova, P. Klodt, and A. Maisky Interaction between alcohol deprivation and morphine withdrawal in mice Drug Alcohol Depend. 34 1993 59 66
91. P.P. Sanna, C. Simpson, R. Lutjens, and G. Koob ERK regulation in chronic ethanol exposure and withdrawal Brain Res. 948 2002 186 191
92. M. Schafer, S.A. Mousa, and C. Stein Corticotropin-releasing factor in antinociception and inflammation Eur. J. Pharmacol. 323 1997 1 10
93. G. Schulteis, A. Markou, M. Cole, and G.F. Koob Decreased brain reward produced by ethanol withdrawal Proc. Natl. Acad. Sci. U S A 92 1995 5880 5884
94. D.W. Self Regulation of drug-taking and -seeking behaviors by neuroadaptations in the mesolimbic dopamine system Neuropharmacology 47 Suppl 1 2004 242 255
95. D.W. Self, and E.J. Nestler Molecular mechanisms of drug reinforcement and addiction Annu. Rev. Neurosci. 18 1995 463 495
96. J.D. Shepard, K.W. Barron, and D.A. Myers Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior Brain Res. 861 2000 288 295
97. J. Shurman, G.F. Koob, and H.B. Gutstein Opioids, pain, the brain, and hyperkatifeia: a framework for the rational use of opioids for pain Pain Med. 11 2010 1092 1098
98. G.R. Siggins, G. Martin, M. Roberto, Z. Nie, S. Madamba, and L. De Lecea Glutamatergic transmission in opiate and alcohol dependence Ann. N. Y. Acad. Sci. 1003 2003 196 211
99. D. Simmons, and D.W. Self Role of mu- and delta-opioid receptors in the nucleus accumbens in cocaine-seeking behavior Neuropsychopharmacology 34 2009 1946 1957
100. G. Simonnet, and C. Rivat Opioid-induced hyperalgesia: abnormal or normal pain? Neuroreport 14 2003 1 7
101. L. Stinus, M. Cador, E.P. Zorrilla, and G.F. Koob Buprenorphine and a CRF1 antagonist block the acquisition of opiate withdrawal-induced conditioned place aversion in rats Neuropsychopharmacology 30 2005 90 98
102. Y. Tache, M. Million, A.G. Nelson, C. Lamy, and L. Wang Role of corticotropin-releasing factor pathways in stress-related alterations of colonic motor function and viscerosensibility in female rodents Gend. Med. 2 2005 146 154
103. D.C. Turk, K.S. Swanson, and R.J. Gatchel Predicting opioid misuse by chronic pain patients: a systematic review and literature synthesis Clin. J. Pain 24 2008 497 508
104. G.R. Valdez, A.J. Roberts, K. Chan, H. Davis, M. Brennan, E.P. Zorrilla, and G.F. Koob Increased ethanol self-administration and anxiety-like behavior during acute ethanol withdrawal and protracted abstinence: regulation by corticotropin-releasing factor Alcohol Clin. Exp. Res. 26 2002 1494 1501
105. G.R. Valdez, E.P. Zorrilla, A.J. Roberts, and G.F. Koob Antagonism of corticotropin-releasing factor attenuates the enhanced responsiveness to stress observed during protracted ethanol abstinence Alcohol 29 2003 55 60
106. T.W. Vanderah, N.M. Suenaga, M.H. Ossipov, T.P. Malan Jr., J. Lai, and F. Porreca Tonic descending facilitation from the rostral ventromedial medulla mediates opioid-induced abnormal pain and antinociceptive tolerance J. Neurosci. 21 2001 279 286
107. L.F. Vendruscolo, J.E. Schlosburg, K.K. Misra, S.A. Chen, T.N. Greenwell, and G.F. Koob Escalation patterns of varying periods of heroin access Pharmacol. Biochem. Behav. 98 2011 570 574
108. B.A. Vogt Pain and emotion interactions in subregions of the cingulate gyrus Nat. Rev. Neurosci. 6 2005 533 544
109. F. Weiss, R. Ciccocioppo, L.H. Parsons, S. Katner, X. Liu, E.P. Zorrilla, G.R. Valdez, O. Ben-Shahar, S. Angeletti, and R.R. Richter Compulsive drug-seeking behavior and relapse. Neuroadaptation, stress, and conditioning factors Ann. N. Y. Acad. Sci. 937 2001 1 26
110. R. West, and M. Gossop Overview: a comparison of withdrawal symptoms from different drug classes Addiction 89 1994 1483 1489
111. H.G. Wolff, J.D. Hardy, and H. Goodell Studies on pain: measurement of the effect of ethyl alcohol on the pain threshold and on the "alarm" reaction J. Pharmacol. 75 1942 38 49
112. A. Yokoyama, T. Takagi, H. Ishii, T. Muramatsu, J. Akai, S. Kato, S. Hori, K. Maruyama, H. Kono, and M. Tsuchiya Impaired autonomic nervous system in alcoholics assessed by heart rate variation Alcohol Clin. Exp. Res. 15 1991 761 765