Jump to ContentJump to Main Navigation
Show Summary Details
In This Section

Translational Neuroscience

1 Issue per year


IMPACT FACTOR 2016: 0.922
5-year IMPACT FACTOR: 1.030

CiteScore 2016: 1.13

SCImago Journal Rank (SJR) 2015: 0.704
Source Normalized Impact per Paper (SNIP) 2015: 0.286

Open Access
Online
ISSN
2081-6936
See all formats and pricing
In This Section

The effect of nucleus accumbens lesions on appetite, sexual function, and nicotine dependence in recovering heroin addicts

Yarong Wang
  • Department of Radiology, Tangdu Hospital, the Fourth Military Medical University, 569 Xinsi Road, Baqiao District, Xi’an, 710038, China
  • Email:
/ Jia Zhu
  • Department of Radiology, Tangdu Hospital, the Fourth Military Medical University, 569 Xinsi Road, Baqiao District, Xi’an, 710038, China
  • Email:
/ Ling Chen
  • Department of Oncology, the First Affiliated Hospital of Xi’an Jiaotong University, 766 West Yantan Road, Xi’an, 710061, China
  • Email:
/ Yijun Liu
  • Department of Psychiatry, University of Florida College of Medicine, 100 Newell Dr L4-100, Gainesville, Florida, 32610, USA
  • Email:
/ Qiang Li
  • Department of Radiology, Tangdu Hospital, the Fourth Military Medical University, 569 Xinsi Road, Baqiao District, Xi’an, 710038, China
  • Email:
/ Weichuan Yang
  • Department of Radiology, Tangdu Hospital, the Fourth Military Medical University, 569 Xinsi Road, Baqiao District, Xi’an, 710038, China
  • Email:
/ Wei Li
  • Department of Radiology, Tangdu Hospital, the Fourth Military Medical University, 569 Xinsi Road, Baqiao District, Xi’an, 710038, China
  • Email:
/ Liyan Zhao
  • National Institute on Drug Dependence, Peking University, 38 Xueyuan Road, Beijing, 100083, China
  • Email:
/ Mark Gold
  • Department of Psychiatry, University of Florida College of Medicine, 100 Newell Dr L4-100, Gainesville, Florida, 32610, USA
  • Email:
/ Jifeng Sun
  • Department of Nephrology, Tangdu Hospital, the Fourth Military Medical University, 569 Xinsi Road, Baqiao District, Xi’an, 710038, China
  • Email:
/ Wei Wang
  • Department of Radiology, Tangdu Hospital, the Fourth Military Medical University, 569 Xinsi Road, Baqiao District, Xi’an, 710038, China
  • Email:
Published Online: 2013-12-20 | DOI: https://doi.org/10.2478/s13380-013-0146-x

Abstract

The nucleus accumbens (NAc) is a key part of the neural circuitry that creates reward, pleasure and motivation that facilitates human feeding, sexual and smoking behaviors. In the brain reward system, the NAc is a crucial component responsible for natural and drug-induced reinforcement behaviors. Yet it is unclear whether NAc is indispensible for all reward behaviors in human beings. The present study aimed to investigate the long-term effects of NAc ablation on sexual function, appetite, and nicotine dependence level in chronic heroin users. Eighteen former heroin-dependent patients (male) with bilateral NAc ablation via stereotactic radiofrequency surgery for alleviating drug psychological dependence were recruited. Their postoperative time ranged from 12 to 103 months. All subjects received MRI scans for assessing the accuracy of the lesion site. Evaluation of appetite, sexual function, and nicotine dependence were measured using the Simplified Nutrition Appetite Questionnaire, the Brief Sexual Function Inventory, and the Fagerström Test for Nicotine Dependence, respectively. After precluding the potential confounding variables, such as drug use (dosage and duration), post-operation duration, age, body-weight, marital status and education level, ANOVA with repeated measures revealed that the NAc ablation improved the patients’ appetite, sexual drive and sexual satisfaction. Yet there was no change in male erectile function, ejaculatory function, or nicotine dependence levels compared to the preoperative. These may suggest that although NAc is a key part of the neural circuitry, the NAc surgical lesions left the fundamental aspects of natural and drug-induced reinforcement and motivation almost intact.

Keywords: Nucleus accumbens (NAc); Heroin dependence; Human reward behavior

  • [1] Spanagel R., Weiss F., The dopamine hypothesis of reward: past and current status, Trends Neurosci., 1999, 22, 521–527 http://dx.doi.org/10.1016/S0166-2236(99)01447-2 [Crossref]

  • [2] Beitner-Johnson D., Nestler E.J., Morphine and cocaine exert common chronic actions on tyrosine hydroxylase in dopaminergic brain reward regions, J. Neurochem., 1991, 57, 344–347 http://dx.doi.org/10.1111/j.1471-4159.1991.tb02133.x [Crossref]

  • [3] Chang J.Y., Janak P.H., Woodward D.J., Comparison of mesocorticolimbic neuronal responses during cocaine and heroin self-administration in freely moving rats, J. Neurosci., 1998, 18, 3098–3115

  • [4] Gerrits M.A., Van Ree J.M., Effect of nucleus accumbens dopamine depletion on motivational aspects involved in initiation of cocaine and heroin self-administration in rats, Brain Res., 1996, 713, 114–124 http://dx.doi.org/10.1016/0006-8993(95)01491-8 [Crossref]

  • [5] Byrnes J.J., Wallace L.J., Amphetamine-induced sensitization and release of dopamine in slices from the ventral tegmental area of rats is enhanced following administration of cholera toxin into the ventral tegmental area, Neurosci. Lett., 1997, 223, 45–48 http://dx.doi.org/10.1016/S0304-3940(97)13399-7 [Crossref]

  • [6] Tassin J.P., Role of dopamine in drug dependence processes [in French], Bull. Acad. Natl. Med., 2002, 186, 295–304, discussion 304-295

  • [7] Due D.L., Huettel S.A., Hall W.G., Rubin D.C., Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging, Am. J. Psychiatry, 2002, 159, 954–960 http://dx.doi.org/10.1176/appi.ajp.159.6.954 [Crossref]

  • [8] Jenkins W.J., Becker J.B., Dynamic increases in dopamine during paced copulation in the female rat, Eur. J. Neurosci., 2003, 18, 1997–2001 http://dx.doi.org/10.1046/j.1460-9568.2003.02923.x [Crossref]

  • [9] Beninger R.J., Bellisle F., Milner P.M., Schedule control of behavior reinforced by electrical stimulation of the brain, Science, 1977, 196, 547–549 http://dx.doi.org/10.1126/science.850798 [Crossref]

  • [10] Alia-Klein N., Parvaz M.A., Woicik P.A., Konova A.B., Maloney T., Shumay E., et al., Gene x disease interaction on orbitofrontal gray matter in cocaine addiction, Arch. Gen. Psychiatry, 2011, 68, 283–294 http://dx.doi.org/10.1001/archgenpsychiatry.2011.10 [Crossref]

  • [11] Volkow N.D., Wang G.J., Fowler J.S., Telang F., Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology, Philos. Trans. R. Soc. Lond. B, 2008, 363, 3191–3200 http://dx.doi.org/10.1098/rstb.2008.0107 [Crossref]

  • [12] Volkow N.D., Fowler J.S., Wang G.J., The addicted human brain: insights from imaging studies, J. Clin. Invest., 2003, 111, 1444–1451 [Crossref]

  • [13] Kiyatkin E.A., Gratton A., Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food, Brain Res., 1994, 652, 225–234 http://dx.doi.org/10.1016/0006-8993(94)90231-3 [Crossref]

  • [14] Villemagne V.L., Wong D.F., Yokoi F., Stephane M., Rice K.C., Matecka D., et al., GBR12909 attenuates amphetamine-induced striatal dopamine release as measured by [(11)C]raclopride continuous infusion PET scans, Synapse, 1999, 33, 268–273 http://dx.doi.org/10.1002/(SICI)1098-2396(19990915)33:4<268::AID-SYN3>3.0.CO;2-W [Crossref]

  • [15] David S.P., Munafo M.R., Johansen-Berg H., Smith S.M., Rogers R.D., Matthews P.M., et al., Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: a functional magnetic resonance imaging study, Biol. Psychiatry, 2005, 58, 488–494 http://dx.doi.org/10.1016/j.biopsych.2005.04.028 [Crossref]

  • [16] Stark R., Schienle A., Girod C., Walter B., Kirsch P., Blecker C., et al., Erotic and disgust-inducing pictures — differences in the hemodynamic responses of the brain, Biol. Psychol., 2005, 70, 19–29 http://dx.doi.org/10.1016/j.biopsycho.2004.11.014 [Crossref]

  • [17] Volkow N.D., Wang G.J., Ma Y., Fowler J.S., Wong C., Jayne M., et al., Effects of expectation on the brain metabolic responses to methylphenidate and to its placebo in non-drug abusing subjects, Neuroimage, 2006, 32, 1782–1792 http://dx.doi.org/10.1016/j.neuroimage.2006.04.192 [Crossref]

  • [18] Zink C.F., Pagnoni G., Martin M.E., Dhamala M., Berns G.S., Human striatal response to salient nonrewarding stimuli, J. Neurosci., 2003, 23, 8092–8097

  • [19] Williams G.V., Rolls E.T., Leonard C.M., Stern C., Neuronal responses in the ventral striatum of the behaving macaque, Behav. Brain Res., 1993, 55, 243–252 http://dx.doi.org/10.1016/0166-4328(93)90120-F [Crossref]

  • [20] Berridge K.C., Food reward: brain substrates of wanting and liking, Neurosci. Biobehav. Rev., 1996, 20, 1–25 http://dx.doi.org/10.1016/0149-7634(95)00033-B [Crossref]

  • [21] Volkow N.D., Wang G.J., Fowler J.S., Tomasi D., Baler R., Food and drug reward: overlapping circuits in human obesity and addiction, Curr. Top. Behav. Neurosci., 2012, 11, 1–24 http://dx.doi.org/10.1007/7854_2011_169 [Crossref]

  • [22] Kippin T.E., Sotiropoulos V., Badih J., Pfaus J.G., Opposing roles of the nucleus accumbens and anterior lateral hypothalamic area in the control of sexual behaviour in the male rat, Eur. J. Neurosci., 2004, 19, 698–704 http://dx.doi.org/10.1111/j.0953-816X.2003.03160.x [Crossref]

  • [23] Carelli R.M., The nucleus accumbens and reward: neurophysiological investigations in behaving animals, Behav. Cogn. Neurosci. Rev., 2002, 1, 281–296 http://dx.doi.org/10.1177/1534582302238338 [Crossref]

  • [24] You Z.B., Chen Y.Q., Wise R.A., Dopamine and glutamate release in the nucleus accumbens and ventral tegmental area of rat following lateral hypothalamic self-stimulation, Neuroscience, 2001, 107, 629–639 http://dx.doi.org/10.1016/S0306-4522(01)00379-7 [Crossref]

  • [25] Volkow N.D., Fowler J.S., Wang G.J., Baler R., Telang F., Imaging dopamine’s role in drug abuse and addiction, Neuropharmacology, 2009, 56, Suppl. 1, 3–8 http://dx.doi.org/10.1016/j.neuropharm.2008.05.022 [Crossref]

  • [26] Mateen F.J., Josephs K.A., Sudden behavioral disturbance in a man with a lesion in the nucleus accumbens, J. Neurol., 2008, 255, 1834–1835 http://dx.doi.org/10.1007/s00415-008-0995-3 [Crossref]

  • [27] Goldenberg G., Schuri U., Gromminger O., Arnold U., Basal forebrain amnesia: does the nucleus accumbens contribute to human memory?, J. Neurol. Neurosurg. Psychiatry, 1999, 67, 163–168 http://dx.doi.org/10.1136/jnnp.67.2.163 [Crossref]

  • [28] Phillips S., Sangalang V., Sterns G., Basal forebrain infarction. A clinicopathologic correlation, Arch. Neurol., 1987, 44, 1134–1138 http://dx.doi.org/10.1001/archneur.1987.00520230024008 [Crossref]

  • [29] Gao G., Wang X., He S., Li W., Wang Q., Liang Q., et al., 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 http://dx.doi.org/10.1159/000075111 [Crossref]

  • [30] Wilson M.M., Thomas D.R., Rubenstein L.Z., Chibnall J.T., Anderson S., Baxi A., et al. Appetite assessment: simple appetite questionnaire predicts weight loss in community-dwelling adults and nursing home residents, Am. J. Clin. Nutr., 2005, 82, 1074–1081

  • [31] Heatherton T.F., Kozlowski L.T., Frecker R.C., Fagerström K.O., The Fagerström Test for Nicotine Dependence: a revision of the Fagerström Tolerance Questionnaire, Br. J. Addict., 1991, 86, 1119–1127 http://dx.doi.org/10.1111/j.1360-0443.1991.tb01879.x [Crossref]

  • [32] Pomerleau C.S., Carton S.M., Lutzke M.L., Flessland K.A., Pomerleau O.F., Reliability of the Fagerström Tolerance Questionnaire and the Fagerström Test for Nicotine Dependence, Addict. Behav., 1994, 19, 33–39 http://dx.doi.org/10.1016/0306-4603(94)90049-3 [Crossref]

  • [33] Radzius A., Moolchan E.T., Henningfield J.E., Heishman S.J., Gallo J.J., A factor analysis of the Fagerström tolerance questionnaire, Addict. Behav., 2001, 26, 303–310 http://dx.doi.org/10.1016/S0306-4603(00)00114-3 [Crossref]

  • [34] O’Leary M.P., Fowler F.J., Lenderking W.R., Barber B., Sagnier P.P., Guess H.A., et al., A brief male sexual function inventory for urology, Urology, 1995, 46, 697–706 http://dx.doi.org/10.1016/S0090-4295(99)80304-5 [Crossref]

  • [35] Shahar S., Charn Y.B., Factors influenceing appetite and depression among institutionalized Chinese elderly in Penang, Malays. J. Health Sci., 2009, 7, 73–88

  • [36] Etter J.F., A comparison of the content-, construct- and predictive validity of the cigarette dependence scale and the Fagerström test for nicotine dependence, Drug Alcohol Depend., 2005, 77, 259–268 http://dx.doi.org/10.1016/j.drugalcdep.2004.08.015 [Crossref]

  • [37] Meneses-Gaya I.C., Zuardi A.W., Loureiro S.R., Crippa J.A., Psychometric properties of the Fagerström Test for Nicotine Dependence, J. Bras. Pneumol., 2009, 35, 73–82 http://dx.doi.org/10.1590/S1806-37132009000100011 [Crossref]

  • [38] Buckley T.C., Mozley S.L., Holohan D.R., Walsh K., Beckham J.C., Kassel J.D., A psychometric evaluation of the Fagerström Test for Nicotine Dependence in PTSD smokers, Addict. Behav., 2005, 30, 1029–1033 http://dx.doi.org/10.1016/j.addbeh.2004.09.005 [Crossref]

  • [39] Fagerström K., Time to first cigarette; the best single indicator of tobacco dependence?, Monaldi Arch. Chest. Dis., 2003, 59, 91–94

  • [40] Dackis C., Gold M.S., Neurotransmitter and neuroendocrine abnormalities associated with cocaine use, Psychiatr. Med., 1985, 3, 461–483

  • [41] Albanese A., Altavista M.C., Rossi P., Organization of central nervous system dopaminergic pathways, J. Neural Transm., 1986, Suppl. 22, 3–17

  • [42] Dahlstroem A., Fuxe K., Evidence for the existence of monoaminecontaining neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons, Acta Physiol. Scand., 1964, Suppl. 232, 231–255

  • [43] Melis M.R., Argiolas A., Dopamine and sexual behavior, Neurosci. Biobehav. Rev., 1995, 19, 19–38 http://dx.doi.org/10.1016/0149-7634(94)00020-2 [Crossref]

  • [44] Everitt B.J., Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats, Neurosci. Biobehav. Rev., 1990, 14, 217–232 http://dx.doi.org/10.1016/S0149-7634(05)80222-2 [Crossref]

  • [45] Liu Y.C., Sachs B.D., Salamone J.D., Sexual behavior in male rats after radiofrequency or dopamine-depleting lesions in nucleus accumbens, Pharmacol. Biochem. Behav., 1998, 60, 585–592 http://dx.doi.org/10.1016/S0091-3057(98)00022-7 [Crossref]

  • [46] Robbins T.W., Cador M., Taylor J.R., Everitt B.J., Limbic-striatal interactions in reward-related processes, Neurosci. Biobehav. Rev., 1989, 13, 155–162 http://dx.doi.org/10.1016/S0149-7634(89)80025-9 [Crossref]

  • [47] Barr B., Leipheimer R.E., Bilateral lesions of the nucleus accumbens do not inhibit copulatory, Soc. Neurosci. Abstr., 1993, 19, 589

  • [48] Pfaus J.G., Kippin T.E., Centeno S., Conditioning and sexual behavior: a review, Horm. Behav., 2001, 40, 291–321 http://dx.doi.org/10.1006/hbeh.2001.1686 [Crossref]

  • [49] Kippin T.E., van der Kooy D., Excitotoxic lesions of the tegmental pedunculopontine nucleus impair copulation in naive male rats and block the rewarding effects of copulation in experienced male rats, Eur. J. Neurosci., 2003, 18, 2581–2591 http://dx.doi.org/10.1046/j.1460-9568.2003.02918.x [Crossref]

  • [50] Bitran D., Hull E.M., Holmes G.M., Lookingland K.J., Regulation of male rat copulatory behavior by preoptic incertohypothalamic dopamine neurons, Brain, Res. Bull., 1988, 20, 323–331 http://dx.doi.org/10.1016/0361-9230(88)90062-7 [Crossref]

  • [51] Stefanick M.L., Davidson J.M., Genital responses in noncopulators and rats with lesions in the medial preoptic area or midthoracic spinal cord, Physiol. Behav., 1987, 41, 439–444 http://dx.doi.org/10.1016/0031-9384(87)90078-3 [Crossref]

  • [52] Cushman P. Jr., Sexual behavior in heroin addiction and methadone maintenance. Correlation with plasma luteinizing hormone, NY State J. Med., 1972, 72, 1261–1265

  • [53] Mintz J., O’Hare K., O’Brien C.P., Goldschmidt J., Sexual problems of heroin addicts, Arch. Gen. Psychiatry, 1974, 31, 700–703 http://dx.doi.org/10.1001/archpsyc.1974.01760170088014 [Crossref]

  • [54] Bang-Ping J., Sexual dysfunction in men who abuse illicit drugs: a preliminary report, J. Sex. Med., 2009, 6, 1072–1080 http://dx.doi.org/10.1111/j.1743-6109.2007.00707.x [Crossref]

  • [55] Roberts L.J., Finch P.M., Pullan P.T., Bhagat C.I., Price L.M., Sex hormone suppression by intrathecal opioids: a prospective study, Clin. J. Pain, 2002, 18, 144–148 http://dx.doi.org/10.1097/00002508-200205000-00002 [Crossref]

  • [56] Mirin S., Meyer R., Mendelson J., Ellingboe J., Opiate use and sexual function, Am. J. Psychiatry, 1980, 137, 909–915

  • [57] Peugh J., Belenko S., Alcohol, drugs and sexual function: a review, J. Psychoactive Drugs, 2001, 33, 223–232 http://dx.doi.org/10.1080/02791072.2001.10400569 [Crossref]

  • [58] Mogenson G.J., Jones D.L., Yim C.Y., From motivation to action: functional interface between the limbic system and the motor system, Prog. Neurobiol., 1980, 14, 69–97 http://dx.doi.org/10.1016/0301-0082(80)90018-0 [Crossref]

  • [59] Zahm D.S., An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens, Neurosci. Biobehav. Rev., 2000, 24, 85–105 http://dx.doi.org/10.1016/S0149-7634(99)00065-2 [Crossref]

  • [60] Shin A.C., Pistell P.J., Phifer C.B., Berthoud H.R., Reversible suppression of food reward behavior by chronic mu-opioid receptor antagonism in the nucleus accumbens, Neuroscience, 2010, 170, 580–588 http://dx.doi.org/10.1016/j.neuroscience.2010.07.017 [Crossref]

  • [61] Beyene M., Carelli R.M., Wightman R.M., Cue-evoked dopamine release in the nucleus accumbens shell tracks reinforcer magnitude during intracranial self-stimulation, Neuroscience, 2010, 169, 1682–1688 http://dx.doi.org/10.1016/j.neuroscience.2010.06.047 [Crossref]

  • [62] Fulton S., Appetite and reward, Front. Neuroendocrinol., 2010, 31, 85–103 http://dx.doi.org/10.1016/j.yfrne.2009.10.003 [Crossref]

  • [63] Berridge K.C., ‘Liking’ and ‘wanting’ food rewards: brain substrates and roles in eating disorders, Physiol. Behav., 2009, 97, 537–550 http://dx.doi.org/10.1016/j.physbeh.2009.02.044 [Crossref]

  • [64] Salamone J.D., Wisniecki A., Carlson B.B., Correa M., Nucleus accumbens dopamine depletions make animals highly sensitive to high fixed ratio requirements but do not impair primary food reinforcement, Neuroscience, 2001, 105, 863–870 http://dx.doi.org/10.1016/S0306-4522(01)00249-4 [Crossref]

  • [65] Salamone J.D., Correa M., Mingote S., Weber S.M., Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse, J. Pharmacol. Exp. Ther., 2003, 305, 1–8 http://dx.doi.org/10.1124/jpet.102.035063 [Crossref]

  • [66] Morabia A., Fabre J., Chee E., Zeger S., Orsat E., Robert A., Diet and opiate addiction: a quantitative assessment of the diet of non-institutionalized opiate addicts, Br. J. Addict., 1989, 84, 173–180 http://dx.doi.org/10.1111/j.1360-0443.1989.tb00566.x [Crossref]

  • [67] Santolaria-Fernández F.J., Gómez-Sirvent J.L., González-Reimers C.E., Batista-López J.N., Jorge-Hernández J.A., Rodríguez-Moreno F., et al., Nutritional assessment of drug addicts, Drug Alcohol Depend., 1995, 38, 11–18 http://dx.doi.org/10.1016/0376-8716(94)01088-3 [Crossref]

  • [68] McCombie L., Elliott L., Farrow K., Gruer L., Morrison A., Cameron J., Injecting drug use and body mass index, Addiction, 1995, 90, 1117–1118 http://dx.doi.org/10.1111/j.1360-0443.1995.tb01071.x [Crossref]

  • [69] Weber R.J., Gomez-Flores R., Smith J.E., Martin T.J., Immune, neuroendocrine, and somatic alterations in animal models of human heroin abuse, J. Neuroimmunol., 2004, 147, 134–137 http://dx.doi.org/10.1016/j.jneuroim.2003.10.029 [Crossref]

  • [70] Forrester J.E., Nutritional alterations in drug abusers with and without HIV, Am. J. Infect. Dis., 2006, 2, 173–179 http://dx.doi.org/10.3844/ajidsp.2006.173.179 [Crossref]

  • [71] Salamone J.D., Correa M., Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine, Behav. Brain Res., 2002, 137, 3–25 http://dx.doi.org/10.1016/S0166-4328(02)00282-6 [Crossref]

  • [72] Hemby S.E., Martin T.J., Co C., Dworkin S.I., Smith J.E., The effects of intravenous heroin administration on extracellular nucleus accumbens dopamine concentrations as determined by in vivo microdialysis, J. Pharmacol. Exp. Ther., 1995, 273, 591–598

  • [73] Devine D.P., Leone P., Pocock D., Wise R.A., Differential involvement of ventral tegmental mu, delta and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies, J. Pharmacol. Exp. Ther., 1993, 266, 1236–1246

  • [74] Hirose N., Murakawa K., Takada K., Oi Y., Suzuki T., Nagase H., et al., Interactions among mu- and delta-opioid receptors, especially putative delta1- and delta2-opioid receptors, promote dopamine release in the nucleus accumbens, Neuroscience, 2005, 135, 213–225 http://dx.doi.org/10.1016/j.neuroscience.2005.03.065 [Crossref]

  • [75] Epstein L.H., Leddy J.J., Food reinforcement, Appetite, 2006, 46, 22–25 http://dx.doi.org/10.1016/j.appet.2005.04.006 [Crossref]

About the article

Published Online: 2013-12-20

Published in Print: 2013-12-01



Citation Information: Translational Neuroscience, ISSN (Online) 2081-6936, ISSN (Print) 2081-3856, DOI: https://doi.org/10.2478/s13380-013-0146-x. Export Citation

© 2013 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. (CC BY-NC-ND 3.0)

Comments (0)

Please log in or register to comment.
Log in