DBS of nucleus accumbens on heroin seeking behaviors in self-administering rats

Drug and Alcohol Dependence

Volumn 129, Issue 1-2, 2013, Pages 70-81

  Guo, Liemei ^a   Zhou, Hongyu ^a   Wang, Ran ^a   Xu, Jiwen ^a   Zhou, Wenhua ^b   Zhang, Fuqiang ^b   Tang, Shuaien ^b   Liu, Huifen ^b   Jiang, Jiyao ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b NINGBO UNIVERSITY   (China)

Author keywords

FosB; CREB; Deep brain stimulation; Drug addiction; Nucleus accumbens; Self administering

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; TRANSCRIPTION FACTOR FOSB;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; ELECTRODE; HELP SEEKING BEHAVIOR; HEROIN DEPENDENCE; IMMUNOHISTOCHEMISTRY; LOCOMOTION; LONG TERM CARE; MALE; MAZE TEST; MENTAL TASK; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RELAPSE; SPATIAL LEARNING; SPATIAL MEMORY; TASK PERFORMANCE; THERAPY EFFECT; TREATMENT DURATION;

ANIMALS; CATHETERIZATION; CONDITIONING, OPERANT; CUES; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DEEP BRAIN STIMULATION; DRUG-SEEKING BEHAVIOR; ELECTRODES, IMPLANTED; HEROIN; HEROIN DEPENDENCE; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAPERITONEAL; MALE; MAZE LEARNING; MOTOR ACTIVITY; NARCOTICS; NUCLEUS ACCUMBENS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; SELF ADMINISTRATION;

RATTUS;

EID: 84875253005     PISSN: 03768716     EISSN: 18790046     Source Type: Journal    
DOI: 10.1016/j.drugalcdep.2012.09.012     Document Type: Article

References (91)

1. Ackermans L., Temel Y., Visser-Vandewalle V. Deep brain stimulation in Tourette's Syndrome. Neurotherapeutics 2008, 5:339-344.
2. Ambroggi F., Ghazizadeh A., Nicola S.M., Fields H.L. Roles of nucleus accumbens core and shell in incentive-cue responding and behavioral inhibition. J. Neurosci. 2011, 31:6820-6830.
3. Arai N., Yokochi F., Ohnishi T., Momose T., Okiyama R., Taniguchi M., Takahashi H., Matsuda H., Ugawa Y. Mechanisms of unilateral STN-DBS in patients with Parkinson's disease: a PET study. J. Neurol. 2008, 2551:1236-1243.
4. Ballanger B., Jahanshahi M., Broussolle E., Thobois S. PET functional imaging of deep brain stimulation in movement disorders and psychiatry. J. Cereb. Blood Flow Metab. 2009, 29:1743-1754.
5. Barrot M., Olivier J.D., Perrotti L.I., DiLeone R.J., Berton O., Eisch A.J., Impey S., Storm D.R., Neve R.L., Yin J.C., Zachariou V., Nestler E.J. CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11435-11440.
6. Berke J.D., Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 2000, 25:515-532.
7. Beurrier C., Bioulac B., Audin J., Hammond C. High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J. Neurophysiol. 2001, 85:1351-1356.
8. Birdno M.J., Grill W.M. Mechanisms of deep brain stimulation in movement disorders as revealed by changes in stimulus frequency. Neurotherapeutics 2008, 5:14-25.
9. Bossert J.M., Stern A.L., Theberge F.R., Marchant N.J., Wang H.L., Morales M., Shaham Y. Role of projections from ventral medial prefrontal cortex to nucleus accumbens shell in context-induced reinstatement of heroin seeking. J. Neurosci. 2012, 32:4982-4991.
10. Bourne S.K., Eckhardt C.A., Sheth S.A., Eskandar E.N. Mechanisms of deep brain stimulation for obsessive compulsive disorder: effects upon cells and circuits. Front. Integr. Neurosci. 2012, 6:29.
11. Bradizza C.M., Stasiewicz P.R., Paas N.D. Relapse to alcohol and drug use among individuals diagnosed with co-occurring mental health and substance use disorders: a review. Clin. Psychol. Rev. 2006, 26:162-178.
12. Carelli R.M., Ijames S.G., Crumling A.J. Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus " natural" (water and food) reward. J. Neurosci. 2000, 20:4255-4266.
13. Carlezon W.A., Thome J., Olson V.G., Lane-Ladd S.B., Brodkin E.S., Hiroi N., Duman R.S., Neve R.L., Nestler E.J. Regulation of cocaine reward by CREB. Science 1998, 282:2272-2275.
14. Chen L.G., Li D.J., Xia X.G., Ming Y., Liu L.T., Liu L., Bao C.S., Bai K.Z., Lan Y.S., Han F.G., Chen Y. A clinical analysis on stereotactic surgery of multi-targets lesion for heroin dependence. Chin. J. Neurosurg. 2005, 21:594-599.
15. Colby C.R., Whisler K., Steffen C., Nestler E.J., Self D.W. Striatal cell type-specific overexpression of DeltaFosB enhances incentive for cocaine. J. Neurosci. 2003, 23:2488-2493.
16. Denys D., Mantione M., Figee M., van den Munckhof P., Koerselman F., Westenberg H., Schuurman R. Deep brain stimulation of the nucleus accumbens for treatment-refractory obsessive-compulsive disorder. Arch. Gen. Psychiatry 2010, 67:1061-1068.
17. Dostrovsky J.O., Levy R., Wu J.P., Hutchison W.D., Tasker R.R., Lozano A.M. Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J. Neurophysiol. 2000, 84:570-574.
18. Epstein D.H., Preston K.L., Stewart J., Shaham Y. Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl.) 2006, 189:1-16.
19. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 2005, 8:1481-1489.
20. Feltenstein M.W., See R.E. The neurocircuitry of addiction: an overview. Br. J. Pharmacol. 2008, 154:261-274.
21. Fingelkurts A., Kahkonen S., Kivisaari R., Borisov S., Puuskari V., Jokela O., Autti T. Reorganization of the composition of brain oscillations and their temporal characteristics during opioid withdrawal. J. Psychopharmacol. 2008, 22:270-284.
22. Flaherty A.W., Williams Z.M., Amirnovin R., Kasper E., Rauch S.L., Cosgrove G.R., Eskandar E.N. Deep brain stimulation of the anterior internal capsule for the treatment of Tourette syndrome: technical case report. Neurosurgery 2005, 57(4 Suppl.):E403.
23. Fuchs R.A., See R.E. Basolateral amygdala inactivation abolishes conditioned stimulus- and heroin-induced reinstatement of extinguished heroin-seeking behavior in rats. Psychopharmacology (Berl.) 2002, 160:425-433.
24. Fuchs R.A., Evans K.A., Parker M.C., See R.E. Differential involvement of the core and shell subregions of the nucleus accumbens in conditioned cue-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl.) 2004, 176:459-465.
25. Fuchs R.A., Ramirez D.R., Bell G.H. Nucleus accumbens shell and core involvement in drug context-induced reinstatement of cocaine seeking in rats. Psychopharmacology (Berl.) 2008, 200:545-556.
26. Gao G., Wang X., He S., Li W., Wang Q., Liang Q., Zhao Y., Hou F., Chen L., Li A. Clinical study for alleviating opiate drug psychological dependence by a method of ablating the nucleus accumbens with stereotactic surgery. Stereotact. Funct. Neurosurg. 2003, 81:96-104.
27. Greenberg B.D., Gabriels L.A., Malone D.A., Rezai A.R., Friehs G.M., Okun M.S., Shapira N.A., Foote K.D., Cosyns P.R., Kubu C.S., Malloy P.F., Salloway S.P., Giftakis J.E., Rise M.T., Machado A.G., Baker K.B., Stypulkowski P.H., Goodman W.K., Rasmussen S.A., Nuttin B.J. Deep brain stimulation of the ventral internal capsule/ventral striatum for obsessive-compulsive disorder: worldwide experience. Mol. Psychiatry 2010, 15:64-79.
28. Guo L.M., Zhou H.Y., Wang R., Zhong Z.H., Xu J.W., Jiang J.Y., Zhou W.H., Zhang F.Q., Tang S.E., Liu H.F. Effects of deep brain stimulation of nucleus accumbens on heroin-seeking behavior in self-administration rats. Chin. J. Stereotact. Funct. Neurosurg. 2010, 23:65-70.
29. Halpern C., Hurtig H., Jaggi J., Grossman M., Won M., Baltuch G. Deep brain stimulation in neurologic disorders. Parkinsonism Relat. Disord. 2007, 13:1-16.
30. Hardesty D.E., Sackeim H.A. Deep brain stimulation in movement and psychiatric disorders. Biol. Psychiatry 2007, 61:831-835.
31. Henderson M.B., Green A.I., Bradford P.S., Chau D.T., Roberts D.W., Leiter J.C. Deep brain stimulation of the nucleus accumbens reduces alcohol intake in alcohol-preferring rats. Neurosurg. Focus 2010, 29:E12.
32. Heng L.J., Wang X.L., Li L.H., Liang Q.C., Li J., Gao G.D. Pathogenesis analysis and therapy of motivation-forming dysfunction after stereotactic surgery for drug abstinence. Chin. J. Neurosurg. 2005, 21:585-589.
33. Horvath T.L., Diano S. The floating blueprint of hypothalamic feeding circuits. Nat. Rev. Neurosci. 2004, 5:662-667.
34. Huff W., Lenartz D., Schormann M., Lee S.H., Kuhn J., Koulousakis A., Mai J., Daumann J., Maarouf M., Klosterkötter J., Sturm V. Unilateral deep brain stimulation of the nucleus accumbens in patients with treatment-resistant obsessive-compulsive disorder: outcomes after one year. Clin. Neurol. Neurosurg. 2010, 112:137-143.
35. Hutcheson D.M., Parkinson J.A., Robbins T.W., Everitt B.J. The effects of nucleus accumbens core and shell lesions on intravenous heroin self-administration and the acquisition of drug-seeking behaviour under a second-order schedule of heroin reinforcement. Psychopharmacology (Berl.) 2001, 153:464-472.
36. Johnson B.D., Brousal J.P., Peterson B.Z., Gallombardo P.A., Hockerman G.H., Lai Y., Scheuer T., Catterall W.A. Modulation of the cloned skeletal muscle L-type Ca2+ channel by anchored cAMP-dependent protein kinase. J. Neurosci. 1997, 17:1243-1255.
37. Kelz M.B., Chen J., Carlezon W.A., Whisler K., Gilden L., Beckmann A.M., Steffen C., Zhang Y.J., Marotti L., Self D.W., Tkatch T., Baranauskas G., Surmeier D.J., Neve R.L., Duman R.S., Picciotto M.R., Nestler E.J. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 1999, 401:272-276.
38. Kilts C.D., Gross R.E., Ely T.D., Drexler K.P. The neural correlates of cue-induced craving in cocaine-dependent women. Am. J. Psychiatry 2004, 161:233-241.
39. Klein J., Winter C., Coquery N., Heinz A., Morgenstern R., Kupsch A., Juckel G. Lesion of the medial prefrontal cortex and the subthalamic nucleus selectively affect depression-like behavior in rats. Behav. Brain Res. 2010, 213:73-81.
40. Knapp C.M., Tozier L., Pak A., Ciraulo D.A., Kornetsky C. Deep brain stimulation of the nucleus accumbens reduces ethanol consumption in rats. Pharmacol. Biochem. Behav. 2009, 92:474-479.
41. Kuhn J., Lenartz D., Mai J.K., Huff W., Lee S.H., Koulousakis A., Klosterkoetter J., Sturm V. Deep brain stimulation of the nucleus accumbens and the internal capsule in therapeutically refractory Tourette-syndrome. J. Neurol. 2007, 254:963-965.
42. Levy D., Shabat-Simon M., Shalev U., Barnea-Ygael N., Cooper A., Zangen A. Repeated electrical stimulation of reward-related brain regions affects cocaine but not " natural" reinforcement. J. Neurosci. 2007, 27:14179-14189.
43. Liu H.Y., Jin J., Tang J.S., Sun W.X., Jia H., Yang X.P., Cui J.M., Wang C.G. Chronic deep brain stimulation in the rat nucleus accumbens and its effect on morphine reinforcement. Addict. Biol. 2008, 13:40-46.
44. Luigjes J., van den Brink W., Feenstra M., van den Munckhof P., Schuurman P.R., Schippers R., Mazaheri A., De Vries T.J., Denys D. Deep brain stimulation in addiction: a review of potential brain targets. Mol. Psychiatry 2012, 17:572-583.
45. Malone D.A., Dougherty D.D., Rezai A.R., Carpenter L.L., Friehs G.M., Eskandar E.N., Rauch S.L., Rasmussen S.A., Machado A.G., Kubu C.S., Tyrka A.R., Price L.H., Stypulkowski P.H., Giftakis J.E., Rise M.T., Malloy P.F., Salloway S.P., Greenberg B.D. Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol. Psychiatry 2009, 65:267-275.
46. McClung C.A., Nestler E.J. Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat. Neurosci. 2003, 6:1208-1215.
47. McCracken C.B., Grace A.A. High-frequency deep brain stimulation of the nucleus accumbens region suppresses neuronal activity and selectively modulates afferent drive in rat orbitofrontal cortex in vivo. J. Neurosci. 2007, 27:12601-12610.
48. McCracken C.B., Grace A.A. Nucleus accumbens deep brain stimulation produces region-specific alterations in local field potential oscillations and evoked responses in vivo. J. Neurosci. 2009, 29:5354-5363.
49. McFarland K., Davidge S.B., Lapish C.C., Kalivas P.W. Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J. Neurosci. 2004, 24:1551-1560.
50. McIntyre C.C., Hahn P.J. Network perspectives on the mechanisms of deep brain stimulation. Neurobiol. Dis. 2010, 38:329-337.
51. Montgomery E.B., Gale J.T. Mechanisms of action of deep brain stimulation (DBS). Neurosci. Biobehav. Rev. 2008, 32:388-407.
52. Mundt A., Klein J., Joel D., Heinz A., Djodari-Irani A., Harnack D., Kupsch A., Orawa H., Juckel G., Morgenstern R., Winter C. High-frequency stimulation of the nucleus accumbens core and shell reduces quinpirole-induced compulsive checking in rats. Eur. J. Neurosci. 2009, 29:2401-2412.
53. Nestler E.J. Molecular mechanisms of drug addiction. Neuropharmacology 2004, 47(Suppl. 1):24-32.
54. Nestler E.J. Transcriptional mechanisms of addiction: role of DeltaFosB. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2008, 363:3245-3255.
55. Orellana C. Controversy over brain surgery for heroin addiction in Russia. Lancet Neurol. 2002, 1:333.
56. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego, pp. 21-23. 3rd ed.
57. Peters J., Kalivas P.W. The group II metabotropic glutamate receptor agonist, LY379268, inhibits both cocaine- and food-seeking behavior in rats. Psychopharmacology (Berl.) 2006, 186:143-149.
58. Pliakas A.M., Carlson R.R., Neve R.L., Konradi C., Nestler E.J., Carlezon W.A. 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. 2001, 21:7397-7403.
59. Qiu J. China clamps down on controversial therapies. Lancet 2009, 373:1834-1835.
60. Schlaepfer T.E., Cohen M.X., Frick C., Kosel M., Brodesser D., Axmacher N., Joe A.Y., Kreft M., Lenartz D., Sturm V. Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 2008, 33:368-377.
61. Schmidt H.D., Anderson S.M., Famous K.R., Kumaresan V., Pierce R.C. Anatomy and pharmacology of cocaine priming-induced reinstatement of drug seeking. Eur. J. Pharmacol. 2005, 526:65-76.
62. Self D.W., Genova L.M., Hope B.T., Barnhart W.J., Spencer J.J., Nestler E.J. Involvement of cAMP-dependent protein kinase in the nucleus accumbens in cocaine self-administration and relapse of cocaine-seeking behavior. J. Neurosci. 1998, 18:1848-1859.
63. Sesia T., Temel Y., Lim L.W., Blokland A., Steinbusch H.W., Visser-Vandewalle V. Deep brain stimulation of the nucleus accumbens core and shell: opposite effects on impulsive action. Exp. Neurol. 2008, 214:135-139.
64. Shen K.Z., Zhu Z.T., Munhall A., Johnson S.W. Synaptic plasticity in rat subthalamic nucleus induced by high-frequency stimulation. Synapse 2003, 50:314-319.
65. Siddiqui M.S., Ellis T.L., Tatter S.B., Okun M.S. Deep brain stimulation: treating neurological and psychiatric disorders by modulating brain activity. NeuroRehabilitation 2008, 23:105-113.
66. Sturm V., Lenartz D., Koulousakis A., Treuer H., Herholz K., Klein J.C., Klosterkötter J. The nucleus accumbens: a target for deep brain stimulation in obsessive-compulsive- and anxiety-disorders. J. Chem. Neuroanat. 2003, 26:293-299.
67. Taba H.A., Wu S.S., Foote K.D., Hass C.J., Fernandez H.H., Malaty I.A., Rodriguez R.L., Dai Y., Zeilman P.R., Jacobson C.E., Okun M.S. A closer look at unilateral versus bilateral deep brain stimulation: results of the National Institutes of Health COMPARE cohort. J. Neurosurg. 2010, 113:1224-1229.
68. Tang Y.L., Liu W.Q., Zhou L.Y., Zhang Y., Zhang Y.S., Kuang P.G., Wang L.G., Luo X.W. The clinical summary of of surgical treatment of 185 patients with heroin dependence. Chin. J. Neurosurg. 2005, 21:600-602.
69. Tye S.J., Frye M.A., Lee K.H. Disrupting disordered neurocircuitry: treating refractory psychiatric illness with neuromodulation. Mayo Clin. Proc. 2009, 84:522-532.
70. Vassoler F.M., Schmidt H.D., Gerard M.E., Famous K.R., Ciraulo D.A., Kornetsky C., Knapp C.M., Pierce R.C. Deep brain stimulation of the nucleus accumbens shell attenuates cocaine priming-induced reinstatement of drug seeking in rats. J. Neurosci. 2008, 28:8735-8739.
71. Volkow N.D., Wang G.J., Fowler J.S., Hitzemann R., Angrist B., Gatley S.J., Logan J., Ding Y.S., Pappas N. Association of methylphenidate-induced craving with changes in right striato-orbitofrontal metabolism in cocaine abusers: implications in addiction. Am. J. Psychiatry 1999, 156:19-26.
72. Volkow N.D., Wang G.J., Ma Y., Fowler J.S., Wong C., Ding Y.S. Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: relevance to addiction. J. Neurosci. 2005, 25:3932-3939.
73. Vorhees C.V., Williams M.T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 2006, 1:848-858.
74. Walker H.C., Watts R.L., Guthrie S., Wang D., Guthrie B.L. Bilateral effects of unilateral subthalamic deep brain stimulation on Parkinson's disease at 1 year. Neurosurgery 2009, 65:302-309.
75. Walters C.L., Blendy J.A. Different requirements for cAMP response element binding protein in positive and negative reinforcing properties of drugs of abuse. J. Neurosci. 2001, 21:9438-9444.
76. Wang G.J., Volkow N.D., Fowler J.S., Cervany P., Hitzemann R.J., Pappas N.R. Regional brain metabolic activation during craving elicited by recall of previous drug experiences. Life Sci. 1999, 64:775-784.
77. Wang J., Ma Y., Huang Z., Sun B., Guan Y., Zuo C. Modulation of metabolic brain function by bilateral subthalamic nucleus stimulation in the treatment of Parkinson's disease. J. Neurol. 2010, 257:72-78.
78. Wang L.L., Wang G.S., Wang Y.Y., Xu J.W., Zhou H.Y., Tian X., Zhao Y.C., Pan X.C. Influence of deep brain stimulation on dopamine receptors in the nucleus accumbens of morphine-dependent rats. Chin. J. Minim. Invasive Neurosurg. 2010, 15:29-32.
79. Wang X.L., He S.M., Heng L.J., Li W.X., Liang Q.C., Li J., Wang J.L., Wang J.T., Gao G.D. Analysis of 1 year follow up results in patients who underwent bilateral nucleus accumbens ablation with stereotactic surgery for the treatment of drug dependence encephalopathy. Chin. J. Neurosurg. 2005, 21:579-584.
80. Wang Y., Zhang F., Tang S., Lai M., Hao W., Zhang Y., Yang J., Zhou W. Lack of effect of habenula lesion on heroin self-administration in rats. Neurosci. Lett. 2009, 461:167-171.
81. Winter C., Lemke C., Sohr R., Meissner W., Harnack D., Juckel G., Morgenstern R., Kupsch A. High frequency stimulation of the subthalamic nucleus modulates neurotransmission in limbic brain regions of the rat. Exp. Brain Res. 2008, 185:497-507.
82. Wyckhuys T., Staelens S., Van Nieuwenhuyse B., Deleye S., Hallez H., Vonck K., Raedt R., Wadman W., Boon P. Hippocampal deep brain stimulation induces decreased rCBF in the hippocampal formation of the rat. Neuroimage 2010, 52:55-61.
83. Xu J.W., Wang G.S., Zhou H.Y., Tian X., Luo Q.Z., Jiang J.Y. Neurosurgical treatment on alleviating heroin psychological dependence. Chin. J. Neurosurg. 2005, 21:590-593.
84. Young C.K., Brown A.R., Robinson J.H., Tuor U.I., Dunn J.F., Bland B.H., Teskey G.C. Functional MRI response and correlated electrophysiological changes during posterior hypothalamic nucleus deep brain stimulation. Neuroimage 2011, 56:35-44.
85. Zachariou V., Bolanos C.A., Selley D.E., Theobald D., Cassidy M.P., Kelz M.B., Shaw-Lutchman T., Berton O., Sim-Selley L.J., Dileone R.J., Kumar A., Nestler E.J. An essential role for DeltaFosB in the nucleus accumbens in morphine action. Nat. Neurosci. 2006, 9:205-211.
86. Zhang F., Zhou W., Tang S., Lai M., Liu H., Yang G. Motivation of heroin-seeking elicited by drug-associated cues is related to total amount of heroin exposure during self-administration in rats. Pharmacol. Biochem. Behav. 2004, 79:291-298.
87. Zhang F. SuperState: a computer program for the control of operant behavioral experimentation. J. Neurosci. Methods 2006, 155:194-201.
88. Zhou H., Xu J., Jiang J. Deep brain stimulation of nucleus accumbens on heroin-seeking behaviors: a case report. Biol. Psychiatry 2011, 69:e41-e42.
89. Zhou W., Zhang F., Tang S., Liu H., Lai M., Yang G. Low dose of heroin inhibits drug-seeking elicited by cues after prolonged withdrawal from heroin self-administration in rats. Neuroreport 2004, 15:727-730.
90. Zhou W., Liu H., Zhang F., Tang S., Zhu H., Lai M., Kalivas P.W. Role of acetylcholine transmission in nucleus accumbens and ventral tegmental area in heroin-seeking induced by conditioned cues. Neuroscience 2007, 144:1209-1218.
91. Zhou W., Kalivas P.W. N-acetylcysteine reduces extinction responding and induces enduring reductions in cue- and heroin-induced drug-seeking. Biol. Psychiatry 2008, 63:338-340.