Norepinephrine at the nexus of arousal, motivation and relapse

Brain Research

Volumn 1641, Issue , 2016, Pages 207-216

  España, Rodrigo A ^a   Schmeichel, Brooke E ^b   Berridge, Craig W ^c  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Addiction; Amphetamine; Catecholamines; Locus coeruleus; Noradrenergic; Stimulants

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; NORADRENALIN; PSYCHOSTIMULANT AGENT;

AFFECT; AROUSAL; BRAIN REGION; COGNITION; DRUG ABUSE; DRUG SEEKING BEHAVIOR; INNERVATION; LOCUS CERULEUS; MOTIVATION; NERVE CELL NETWORK; NEUROANATOMY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RELAPSE; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; DRUG DEPENDENCE; HUMAN; METABOLISM; PHYSIOLOGY; RECURRENT DISEASE;

ANIMALS; AROUSAL; BRAIN; DRUG-SEEKING BEHAVIOR; HUMANS; MOTIVATION; NOREPINEPHRINE; RECURRENCE; SUBSTANCE-RELATED DISORDERS;

EID: 84962128023     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2016.01.002     Document Type: Review

References (106)

1. E.D. Abercrombie, and B.L. Jacobs Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. II. Adaptation to chronically presented stressful stimuli J. Neurosci. 7 1987 2844 2848
2. Z. Amit, Z.W. Brown, D.E. Levitan, and S.O. Ogren Noradrenergic mediation of the positive reinforcing properties of ethanol: I. Suppression of ethanol consumption in laboratory rats following dopamine-beta-hydroxylase inhibition Arch. Int. Pharmacodyn. Ther. 230 1977 65 75
3. A.F. Arnsten, and P.S. Goldman-Rakic Selective prefrontal cortical projections to the region of the locus coeruleus and raphe nuclei in the rhesus monkey Brain Res. 306 1984 9 18
4. A.F. Arnsten, J.C. Steere, and R.D. Hunt The contribution of alpha 2-noradrenergic mechanisms of prefrontal cortical cognitive function. Potential significance for attention-deficit hyperactivity disorder Arch. Gen. Psychiatry 53 1996 448 455
5. G. Aston-Jones, and F.E. Bloom Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle J. Neurosci. 1 1981 876 886
6. T.B. Baker, M.E. Piper, D.E. McCarthy, M.R. Majeskie, and M.C. Fiore Addiction motivation reformulated: an affective processing model of negative reinforcement Psychol. Rev. 111 2004 33 51
7. C.W. Berridge, and S.L. Foote Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus J. Neurosci. 11 1991 3135 3145
8. C.W. Berridge, M.E. Page, R.J. Valentino, and S.L. Foote Effects of locus coeruleus inactivation on electroencephalographic activity in neocortex and hippocampus Neuroscience 55 1993 381 393
9. C.W. Berridge, S.J. Bolen, M.S. Manley, and S.L. Foote Modulation of forebrain electroencephalographic activity in halothane-anesthetized rat via actions of noradrenergic beta-receptors within the medial septal region J. Neurosci. 16 1996 7010 7020
10. C.W. Berridge, and S.L. Foote Enhancement of behavioral and electroencephalographic indices of waking following stimulation of noradrenergic beta-receptors within the medial septal region of the basal forebrain J. Neurosci. 16 1996 6999 7009
11. C.W. Berridge, J. O'Neil, and K. Wifler Amphetamine acts within the medial basal forebrain to initiate and maintain alert waking Neuroscience 93 1999 885 896
12. C.W. Berridge, and R.A. España Synergistic sedative effects of noradrenergic alpha(1)- and beta- receptor blockade on forebrain electroencephalographic and behavioral indices Neuroscience 99 2000 495 505
13. C.W. Berridge, and M.F. Morris Amphetamine-induced activation of forebrain EEG is prevented by noradrenergic beta-receptor blockade in the halothane-anesthetized rat Psychopharmacology 148 2000 307 313
14. C.W. Berridge, and J. O'Neill Differential sensitivity to the wake-promoting actions of norepinephrine within the medial preoptic area and the substantia innominata Behav. Neurosci. 115 2001 165 174
15. C.W. Berridge, and T.A. Stalnaker Relationship between low-dose amphetamine-induced arousal and extracellular norepinephrine and dopamine levels within prefrontal cortex Synapse 46 2002 140 149
16. C.W. Berridge, S.O. Isaac, and R.A. España Additive wake-promoting actions of medial basal forebrain noradrenergic alpha1- and beta-receptor stimulation Behav. Neurosci. 117 2003 350 359
17. C.W. Berridge, and B.D. Waterhouse The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes Brain Res. Brain Res. Rev. 42 2003 33 84
18. C.W. Berridge, B.E. Schmeichel, and R.A. España Noradrenergic modulation of wakefulness/arousal Sleep Med. Rev. 16 2012 187 197
19. K.C. Berridge, and T.E. Robinson Parsing reward Trends Neurosci. 26 2003 507 513
20. Z.J. Brown, E. Tribe, N. D'Souza, and A. Erb, S. Interaction between noradrenaline and corticotrophin-releasing factor in the reinstatement of cocaine seeking in the rat Psychopharmacology 203 2009 121 130
21. Z.J. Brown, J.N. Nobrega, and S. Erb Central injections of noradrenaline induce reinstatement of cocaine seeking and increase c-fos mRNA expression in the extended amygdala Behav. Brain Res. 217 2011 472 476
22. Z.W. Brown, Z. Amit, D.E. Levitan, S.O. Ogren, and E.A. Sutherland Noradrenergic mediation of the positive reinforcing properties of ethanol: II. Extinction of ethanol-drinking behavior in laboratory rats by inhibition of dopamine-beta-hydroxylase. Implications for treatment procedures in human alcoholics Arch. Int. Pharmacodyn. Ther. 230 1977 76 82
23. Z.W. Brown, Z. Amit, D. Sinyor, G.E. Rockman, and S.O. Ogren Suppression of voluntary ingestion of morphine by inhibition of dopamine-beta-hydroxylase Arch. Int. Pharmacodyn. Ther. 232 1978 102 110
24. G. Buzsaki, L.W. Leung, and C.H. Vanderwolf Cellular bases of hippocampal EEG in the behaving rat Brain Res. 287 1983 139 171
25. G. Buzsaki, R.G. Bickford, G. Ponomareff, L.J. Thal, R. Mandel, and F.H. Gage Nucleus basalis and thalamic control of neocortical activity in the freely moving rat J. Neurosci. 8 1988 4007 4026
26. G. Buzsaki, and F.H. Gage The cholinergic nucleus basalis: a key structure in neocortical arousal EXS. 57 1989 159 171
27. E.G. Cape, and B.E. Jones Differential modulation of high-frequency gamma-electroencephalogram activity and sleep-wake state by noradrenaline and serotonin microinjections into the region of cholinergic basalis neurons J. Neurosci. 18 1998 2653 2666
28. M.E. Carter, O. Yizhar, S. Chikahisa, H. Nguyen, A. Adamantidis, S. Nishino, K. Deisseroth, and L. de Lecea Tuning arousal with optogenetic modulation of locus coeruleus neurons Nat. Neurosci. 13 2010 1526 1533
29. D.A. Cooper, H.L. Kimmel, D.F. Manvich, K.T. Schmidt, D. Weinshenker, and L.L. Howell Effects of pharmacologic dopamine beta-hydroxylase inhibition on cocaine-induced reinstatement and dopamine neurochemistry in squirrel monkeys J. Pharmacol. Exp. Ther. 350 2014 144 152
30. W.E. Cullinan, and L. Zaborszky Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons J. Comp. Neurol. 306 1991 631 667
31. D.F. Cummings, S.S. Ericksen, A. Goetz, and J.A. Schetz Transmembrane Segment Five Serines of the D4 Dopamine Receptor Uniquely Influence the Interactions of Dopamine, Norepinephrine, and Ro10-4548 J. Pharmacol. Exp. Ther. 333 2010 682 695
32. C. Drouin, L. Darracq, F. Trovero, G. Blanc, J. Glowinski, S. Cotecchia, and J.P. Tassin Alpha1b-adrenergic receptors control locomotor and rewarding effects of psychostimulants and opiates J. Neurosci. 22 2002 2873 2884
33. A.J. Dunn Stress-related changes in cerebral catecholamine and indoleamine metabolism: lack of effect of adrenalectomy and corticosterone J. Neurochem. 51 1988 406 412
34. S. Erb, P.K. Hitchcott, H. Rajabi, D. Mueller, Y. Shaham, and J. Stewart Alpha-2 adrenergic receptor agonists block stress-induced reinstatement of cocaine seeking Neuropsychopharmacology 23 2000 138 150
35. España, R.A.; Vlasaty, J.; McCormack, S.L.; Llewellyn-Smith, I.J.; Scammell, T.E.; 2005. Aminergic inputs to the hypocretin/orexin neurons. Society for Neuroscience Meeting.
36. R.A. España, and C.W. Berridge Organization of noradrenergic efferents to arousal-related basal forebrain structures J. Comp. Neurol. 496 2006 668 683
37. M.K. Fitzgerald, J.M. Otis, and D. Mueller Dissociation of beta1- and beta2-adrenergic receptor subtypes in the retrieval of cocaine-associated memory Behav. Brain Res. 296 2016 94 99
38. S.M. Florin, R. Kuczenski, and D.S. Segal Regional extracellular norepinephrine responses to amphetamine and cocaine and effects of clonidine pretreatment Brain Res. 654 1994 53 62
39. S.M. Florin, R. Kuczenski, and D.S. Segal Effects of reserpine on extracellular caudate dopamine and hippocampus norepinephrine responses to amphetamine and cocaine: mechanistic and behavioral considerations J. Pharmacol. Exp. Ther. 274 1995 231 241
40. S.L. Foote, G. Aston-Jones, and F.E. Bloom Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal Proc. Natl. Acad. Sci. USA 77 1980 3033 3037
41. S.L. Foote, F.E. Bloom, and G. Aston-Jones Nucleus locus ceruleus: new evidence of anatomical and physiological specificity Physiol. Rev. 63 1983 844 914
42. O. George, and G.F. Koob Individual differences in prefrontal cortex function and the transition from drug use to drug dependence Neurosci. Biobehav. Rev. 35 2010 232 247
43. N.W. Gilpin, and G.F. Koob Effects of beta-adrenoceptor antagonists on alcohol drinking by alcohol-dependent rats Psychopharmacology 212 2010 431 439
44. S.R. Goldberg, and F.A. Gonzalez Effects of propranolol on behavior maintained under fixed-ratio schedules of cocaine injection or food presentation in squirrel monkeys J. Pharmacol. Exp. Ther. 198 1976 626 634
45. T.H. Hand, L. Stinus, and M. Le Moal Differential mechanisms in the acquisition and expression of heroin-induced place preference Psychopharmacology 98 1989 61 67
46. G.C. Harris, M.A. Hedaya, W.J. Pan, and P. Kalivas beta-adrenergic antagonism alters the behavioral and neurochemical responses to cocaine Neuropsychopharmacology 14 1996 195 204
47. D. Highfield, A. Clements, U. Shalev, R. McDonald, R. Featherstone, J. Stewart, and Y. Shaham Involvement of the medial septum in stress-induced relapse to heroin seeking in rats Eur. J. Neurosci. 12 2000 1705 1713
48. J.A. Hobson, R.W. McCarley, and P.W. Wyzinski Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups Science 189 1975 55 58
49. M.L. Jobes, U.E. Ghitza, D.H. Epstein, K.A. Phillips, S.J. Heishman, and K.L. Preston Clonidine blocks stress-induced craving in cocaine users Psychopharmacology 218 2011 83 88
50. P.W. Kalivas, and K. McFarland Brain circuitry and the reinstatement of cocaine-seeking behavior Psychopharmacology 168 2003 44 56
51. H. Kleinlogel, G. Scholtysik, and A.C. Sayers Effects of clonidine and BS 100-141 on the EEG sleep pattern in rats Eur. J. Pharmacol. 33 1975 159 163
52. G.F. Koob Stress, corticotropin-releasing factor, and drug addiction Ann. N Y. Acad. Sci. 897 1999 27 45
53. T.R. Kosten, B.J. Rounsaville, and H.D. Kleber A 2.5-year follow-up of depression, life crises, and treatment effects on abstinence among opioid addicts Arch. Gen. Psychiatry 43 1986 733 738
54. R. Kuczenski, and D.S. Segal Regional norepinephrine response to amphetamine using dialysis: comparison with caudate dopamine Synapse 11 1992 164 169
55. V. Kumar, S. Datta, G.S. Chhina, N. Gandhi, and B. Singh Sleep-awake responses elicited from medial preoptic area on application of norepinephrine and phenoxybenzamine in free moving rats Brain Res. 322 1984 322 325
56. V.M. Kumar, S. Datta, G.S. Chhina, and B. Singh Alpha adrenergic system in medial preoptic area involved in sleep-wakefulness in rats Brain Res. Bull. 16 1986 463 468
57. R. Laverty, and K.M. Taylor Behavioural and biochemical effects of 2-(2,6-dichlorophenylamino)-2-imidazoline hydrochloride (St 155) on the central nervous system Br. J. Pharmacol. 35 1969 253 264
58. A.D. Lê, S. Harding, W. Juzytsch, J. Watchus, U. Shalev, and Y. Shaham The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats Psychopharmacology 150 2000 317 324
59. A.D. Lê, S. Harding, W. Juzytsch, D. Funk, and Y. Shaham Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats Psychopharmacology 179 2005 366 373
60. A.D. Lê, D. Funk, S. Harding, W. Juzytsch, P.J. Fletcher, and Y. Shaham Effects of dexfenfluramine and 5-HT3 receptor antagonists on stress-induced reinstatement of alcohol seeking in rats Psychopharmacology 186 2006 82 92
61. A.D. Lê, D. Funk, S. Harding, W. Juzytsch, and P.J. Fletcher The role of noradrenaline and 5-hydroxytryptamine in yohimbine-induced increases in alcohol-seeking in rats Psychopharmacology 204 2009 477 488
62. A.D. Lê, D. Funk, W. Juzytsch, K. Coen, B.M. Navarre, C. Cifani, and Y. Shaham Effect of prazosin and guanfacine on stress-induced reinstatement of alcohol and food seeking in rats Psychopharmacology 218 2011 89 99
63. M.G. Lee, I.D. Manns, A. Alonso, and B.E. Jones Sleep-wake related discharge properties of basal forebrain neurons recorded with micropipettes in head-fixed rats J. Neurophysiol. 92 2004 1182 1198
64. F. Leri, J. Flores, D. Rodaros, and J. Stewart Blockade of stress-induced but not cocaine-induced reinstatement by infusion of noradrenergic antagonists into the bed nucleus of the stria terminalis or the central nucleus of the amygdala J. Neurosci. 22 2002 5713 5718
65. J.R. Mantsch, A. Weyer, O. Vranjkovic, C.E. Beyer, D.A. Baker, and H. Caretta Involvement of noradrenergic neurotransmission in the stress- but not cocaine-induced reinstatement of extinguished cocaine-induced conditioned place preference in mice: role for beta-2 adrenergic receptors Neuropsychopharmacology 35 2010 2165 2178
66. J.R. Mantsch, O. Vranjkovic, R.C. Twining, P.J. Gasser, J.R. McReynolds, and J.M. Blacktop Neurobiological mechanisms that contribute to stress-related cocaine use Neuropharmacology 76 2014 383 394
67. J.R. Mantsch, D.A. Baker, D. Funk, A.D. Le, and Y. Shaham Stress-induced reinstatement of drug seeking: 20 years of progress Neuropsychopharmacology 2015
68. A.T. McLellan, D.C. Lewis, C.P. O'Brien, and H.D. Kleber Drug dependence, a chronic medical illness: implications for treatment, insurance, and outcomes evaluation JAMA 284 2000 1689 1695
69. R. Metherate, C.L. Cox, and J.H. Ashe Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine J. Neurosci. 12 1992 4701 4711
70. A. Newman-Tancredi, V. Audinot-Bouchez, A. Gobert, and M.J. Millan Noradrenaline and adrenaline are high affinity agonists at dopamine D4 receptors Eur. J. Pharmacol. 319 1997 379 383
71. V.G. Olson, C.L. Heusner, R.J. Bland, M.J. During, D. Weinshenker, and R.D. Palmiter Role of noradrenergic signaling by the nucleus tractus solitarius in mediating opiate reward Science 311 2006 1017 1020
72. R.H. Pastel, and J.D. Fernstrom The effects of clonidine on EEG wavebands associated with sleep in the rat Brain Res. 300 1984 243 255
73. D.M. Platt, J.K. Rowlett, and R.D. Spealman Noradrenergic mechanisms in cocaine-induced reinstatement of drug seeking in squirrel monkeys J. Pharmacol. Exp. Ther. 322 2007 894 902
74. J.S. Richardson, and D.M. Novakovski Brain monoamines and free choice ethanol consumption in rats Drug Alcohol Depend. 3 1978 253 264
75. D.C.S. Roberts, M.E. Corcoran, and H.C. Fibiger On the role of ascending catecholaminergic systems in intravenous self-administration of cocaine Pharmacol. Biochem. Behav. 6 1977 615 620
76. S.D. Robertson, N.W. Plummer, J. de Marchena, and P. Jensen Developmental origins of central norepinephrine neuron diversity Nat. Neurosci. 16 2013 1016 1023
77. B.A. Rocha Stimulant and reinforcing effects of cocaine in monoamine transporter knockout mice Eur. J. Pharmacol. 479 2003 107 115
78. H. Sahraei, H. Ghazzaghi, M.R. Zarrindast, H. Ghoshooni, H. Sepehri, and A. Haeri-Rohan The role of alpha-adrenoceptor mechanism(s) in morphine-induced conditioned place preference in female mice Pharmacol. Biochem. Behav. 78 2004 135 141
79. J.D. Salamone, and M. Correa The mysterious motivational functions of mesolimbic dopamine Neuron 76 2012 470 485
80. J.D. Salamone, M. Correa, E.J. Nunes, P.A. Randall, and M. Pardo The behavioral pharmacology of effort-related choice behavior: dopamine, adenosine and beyond J. Exp. Anal. Behav. 97 2012 125 146
81. J.R. Schank, R. Ventura, S. Puglisi-Allegra, A. Alcaro, C.D. Cole, L.C. Liles, P. Seeman, and D. Weinshenker Dopamine beta-hydroxylase knockout mice have alterations in dopamine signaling and are hypersensitive to cocaine Neuropsychopharmacology 31 2006 2221 2230
82. B.E. Schmeichel, and C.W. Berridge Wake-promoting actions of noradrenergic alpha1-and beta-receptors within the lateral hypothalamic area Eur. J. Neurosci. 37 2013 891 900
83. B.E. Schmeichel, and C.W. Berridge Amphetamine acts within the lateral hypothalamic area to elicit affectively neutral arousal and reinstate drug-seeking Int. J. Neuropsychopharmacol. 17 2014 63 75
84. J.P. Schroeder, S.A. Epps, T.W. Grice, and D. Weinshenker The selective dopamine beta-hydroxylase inhibitor nepicastat attenuates multiple aspects of cocaine-seeking behavior Neuropsychopharmacology 38 2013 1032 1038
85. W. Schultz Neuronal reward and decision signals: from theories to data Physiol. Rev. 95 2015 853 951
86. D.W. Self Regulation of drug-taking and -seeking behaviors by neuroadaptations in the mesolimbic dopamine system Neuropharmacology 47 Suppl 1 2004 S242 S255
87. Y. Shaham, S. Erb, and J. Stewart Stress-induced relapse to heroin and cocaine seeking in rats: a review Brain Res. Brain Res. Rev. 33 2000 13 33
88. Y. Shaham, D. Highfield, J. Delfs, S. Leung, and J. Stewart Clonidine blocks stress-induced reinstatement of heroin seeking in rats: an effect independent of locus coeruleus noradrenergic neurons Eur. J. Neurosci. 12 2000 292 302
89. R. Sinha, A. Kimmerling, C. Doebrick, and T.R. Kosten Effects of lofexidine on stress-induced and cue-induced opioid craving and opioid abstinence rates: preliminary findings Psychopharmacology 190 2007 569 574
90. M.J. Skelly, and J.L. Weiner Chronic treatment with prazosin or duloxetine lessens concurrent anxiety-like behavior and alcohol intake: evidence of disrupted noradrenergic signaling in anxiety-related alcohol use Brain Behav. 4 2014 468 483
91. S. Sood, J.K. Dhawan, V. Ramesh, J. John, G. Gopinath, and V.M. Kumar Role of medial preoptic area beta adrenoceptors in the regulation of sleep-wakefulness Pharmacol. Biochem. Behav. 57 1997 1 5
92. J. Stewart Pathways to relapse: the neurobiology of drug- and stress-induced relapse to drug-taking J. Psychiatry Neurosci. 25 2000 125 136
93. L.W. Swanson, and B.K. Hartman The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker J. Comp. Neurol. 163 1975 467 505
94. R. Ventura, S. Cabib, A. Alcaro, C. Orsini, and S. Puglisi-Allegra Norepinephrine in the prefrontal cortex is critical for amphetamine-induced reward and mesoaccumbens dopamine release J. Neurosci. 23 2003 1879 1885
95. R. Ventura, A. Alcaro, and S. Puglisi-Allegra Prefrontal cortical norepinephrine release is critical for morphine-induced reward, reinstatement and dopamine release in the nucleus accumbens Cereb. Cortex 15 2005 1877 1886
96. S. Wee, Z. Wang, R. He, J. Zhou, A.P. Kozikowski, and W.L. Woolverton Role of the increased noradrenergic neurotransmission in drug self-administration Drug. Alcohol Depend. 82 2006 151 157
97. D. Weinshenker, N.C. Rust, N.S. Miller, and R.D. Palmiter Ethanol-associated behaviors of mice lacking norepinephrine J. Neurosci. 20 2000 3157 3164
98. D. Weinshenker, and J.P. Schroeder There and back again: a tale of norepinephrine and drug addiction Neuropsychopharmacology 32 2007 1433 1451
99. F. Xu, R.R. Gainetdinov, W.C. Wetsel, S.R. Jones, L.M. Bohn, G.W. Miller, Y.M. Wang, and M.G. Caron Mice lacking the norepinephrine transporter are supersensitive to psychostimulants Nat. Neurosci. 3 2000 465 471
100. R.M. Yerkes, and J.D. Dodson The relation of strength of stimulus to rapidity of habit-formation J. Comp. Neurol. Psychol. 18 1908 459 482
101. K. Yoshida, S. McCormack, R.A. España, A. Crocker, and T.E. Scammell Afferents to the orexin neurons of the rat brain J. Comp. Neurol. 494 2006 845 861
102. L. Zaborszky Afferent connections of the forebrain cholinergic projection neurons, with special reference to monoaminergic and peptidergic fibers Exs 57 1989 12 32
103. L. Zaborszky, W.E. Cullinan, and A. Braun Afferents to basal forebrain cholinergic projection neurons: an update Adv. Exp. Med. Biol. 295 1991 43 100
104. L. Zaborszky, and W.E. Cullinan Direct catecholaminergic-cholinergic interactions in the basal forebrain. I. Dopamine-beta-hydroxylase- and tyrosine hydroxylase input to cholinergic neurons J. Comp. Neurol. 374 1996 535 554
105. M.R. Zarrindast, T. Bahreini, and M. Adl Effect of imipramine on the expression and acquisition of morphine-induced conditioned place preference in mice Pharmacol. Biochem. Behav. 73 2002 941 949
106. X.Y. Zhang, and T.A. Kosten Prazosin, an alpha-1 adrenergic antagonist, reduces cocaine-induced reinstatement of drug-seeking Biol. Psychiatry 57 2005 1202 1204