Voluntary ethanol intake predicts κ-opioid receptor supersensitivity and regionally distinct dopaminergic adaptations in macaques

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 5959-5968

  Siciliano, Cody A ^a   Calipari, Erin S ^a   Cuzon Carlson, Verginia C ^b   Helms, Christa M ^b   Lovinger, David M ^c   Grant, Kathleen A ^b   Jones, Sara R ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Caudate; Dopamine; Nonhuman primate; Nucleus accumbens; Voltammetry; opioid receptor

Indexed keywords

DOPAMINE; DOPAMINE TRANSPORTER; KAPPA OPIATE RECEPTOR; ALCOHOL; CENTRAL DEPRESSANT AGENT;

ADAPTATION; ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATOGRAPHY; CONTROLLED STUDY; CORPUS STRIATUM; CORRELATION ANALYSIS; DOPAMINE RELEASE; DOPAMINE UPTAKE; DOPAMINERGIC ACTIVITY; DRINKING BEHAVIOR; MACACA FASCICULARIS; MALE; NONHUMAN; NUCLEUS ACCUMBENS; POST HOC ANALYSIS; POTENTIOMETRY; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SUPERSENSITIVITY; TISSUE PREPARATION; ANIMAL; BLOOD; CAUDATE NUCLEUS; DRUG SELF ADMINISTRATION; ELECTROCHEMISTRY; METABOLISM; NONPARAMETRIC TEST; PATHOPHYSIOLOGY;

ALCOHOL DRINKING; ANIMALS; CAUDATE NUCLEUS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOPAMINE; ELECTROCHEMISTRY; ETHANOL; MACACA FASCICULARIS; MALE; NUCLEUS ACCUMBENS; RECEPTORS, OPIOID, KAPPA; SELF ADMINISTRATION; STATISTICS, NONPARAMETRIC;

EID: 84929259721     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4820-14.2015     Document Type: Article

References (51)

1. Bazov I, Kononenko O, Watanabe H, Kuntić V, Sarkisyan D, Taqi MM, Hussain MZ, Nyberg F, Yakovleva T, Bakalkin G (2013) The endogenous opioid system in human alcoholics: molecular adaptations in brain areas involved in cognitive control of addiction. Addict Biol 18:161-169. CrossRef Medline
2. Belin D, Everitt BJ (2008) Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57:432-441. CrossRef Medline
3. Berger AL, Williams AM, McGinnis MM, Walker BM (2013) Affective cue-induced escalation of alcohol self-administration and increased 22-kHz ultrasonic vocalizations during alcohol withdrawal: role of kappa-opioid receptors. Neuropsychopharmacology 38:647-654. CrossRef Medline
4. Bossert JM, Poles GC, Wihbey KA, Koya E, Shaham Y (2007) Differential effects of blockade of dopamine DI-family receptors in nucleus accum-bens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues. J Neurosci 27:12655-12663. CrossRef Medline
5. Carelli RM (2002) The nucleus accumbens and reward: neurophysiological investigations in behaving animals. Behav Cogn Neurosci Rev 1:281-296. CrossRef Medline
6. Collins SL, Gerdes RM, D’Addario C, Izenwasser S (2001) Kappa opioid agonists alter dopamine markers and cocaine-stimulated locomotor activity. Behav Pharmacol 12:237-245. CrossRef Medline
7. Cuzon Carlson VC, Seabold GK, Helms CM, Garg N, Odagiri M, Rau AR, Daunais J, Alvarez VA, Lovinger DM, Grant KA (2011) Synaptic and morphological neuroadaptations in the putamen associated with longterm, relapsing alcohol drinking in primates. Neuropsychopharmacology 36:2513-2528. CrossRef Medline
8. Das D, Rogers J, Michael-Titus AT (1994) Comparative study of the effects of mu, delta and kappa opioid agonists on 3H-dopamine uptake in rat striatum and nucleus accumbens. Neuropharmacology 33:221-226. CrossRef Medline
9. Daunais JB, Kraft RA, Davenport AT, Burnett EJ, Maxey VM, Szeliga KT, Rau AR, Flory GS, Hemby SE, Kroenke CD, Grant KA, Friedman DP (2010) MRI-guided dissection of the nonhuman primate brain: a case study. Methods 50:199-204. CrossRef Medline
10. Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137:75-114. Medline
11. Ebner SR, Roitman MF, Potter DN, Rachlin AB, Chartoff EH (2010) Depressive-like effects of the kappa opioid receptor agonist salvinorin A are associated with decreased phasic dopamine release in the nucleus accumbens. Psychopharmacology (Berl) 210:241-252. CrossRef
12. Enoch MA (2011) The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology (Berl) 214:17-31. CrossRef
13. Everitt BJ, Robbins TW (2013) From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci Biobehav Rev 37:1946-1954. Medline
14. Ferris MJ, Calipari ES, Yorgason JT, Jones SR (2013) Examining the complex regulation and drug-induced plasticity of dopamine release and uptake using voltammetry in brain slices. ACS Chem Neurosci 4:693-703. CrossRef Medline
15. Ferris MJ, España RA, Locke JL, Konstantopoulos JK, Rose JH, Chen R, Jones SR (2014) Dopamine transporters govern diurnal variation in extracellular dopamine tone. Proc Natl Acad Sci USA 111:E2751-E2759. CrossRef Medline
16. Gehrke BJ, Chefer VI, Shippenberg TS (2008) Effects of acute and repeated administration of salvinorin A on dopamine function in the rat dorsal striatum. Psychopharmacology (Berl) 197:509-517. CrossRef
17. Grant KA, Leng X, Green HL, Szeliga KT, Rogers LS, Gonzales SW (2008) Drinking typography established by scheduled induction predicts chronic heavy drinking in a monkey model of ethanol self-administration. Alcohol Clin Exp Res 32:1824-1838. CrossRef Medline
18. Grant KA, Ferguson B, Helms CM, McClintick MN (2014) Drinking to dependence risk factors in nonhuman primates. In: Neurobiology of alcohol dependence (Noronha AB, Cui C, Harris RA, Crabbe JC, eds), pp 412-424. Waltham, MA: Elsevier.
19. Graybiel AM (1995) The basal ganglia. Trends Neurosci 18:60-62. Medline
20. Graybiel AM (2008) Habits, rituals, and the evaluative brain. Annu Rev Neurosci 31:359-387. CrossRef Medline
21. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991) Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89-125. CrossRef Medline
22. Kelly RS, Wightman RM (1987) Detection of dopamine overflow and diffusion with voltammetry in slices of rat brain. Brain Res 423:79-87. Medline
23. Kissler JL, Sirohi S, Reis DJ, Jansen HT, Quock RM, Smith DG, Walker BM (2014) The one-two punch of alcoholism: role of central amygdala dynorphins/kappa-opioid receptors. Biol Psychiatry 75:774-782. CrossRef Medline
24. Kivell B, Uzelac Z, Sundaramurthy S, Rajamanickam J, Ewald A, Chefer V, Jaligam V, Bolan E, Simonson B, Annamalai B, Mannangatti P, Prisin-zano TE, Gomes I, Devi LA, Jayanthi LD, Sitte HH, Ramamoorthy S, Shippenberg TS (2014) Salvinorin A regulates dopamine transporter function via a kappa opioid receptor and ERK1/2-dependent mechanism. Neuropharmacology 86:228-240. CrossRef Medline
25. Le Merrer J, Becker JA, Befort K, Kieffer BL (2009) Reward processing by the opioid system in the brain. Physiol Rev 89:1379-1412. CrossRef Medline
26. Lemos JC, Wanat MJ, Smith JS, Reyes BA, Hollon NG, Van Bockstaele EJ, Chavkin C, Phillips PE (2012) Severe stress switches CRF action in the nucleus accumbens from appetitive to aversive. Nature 490:402-406. CrossRef Medline
27. Lindholm S, Rosin A, Dahlin I, Georgieva J, Franck J (2007) Ethanol alters the effect of kappa receptor ligands on dopamine release in the nucleus accumbens. Physiol Behav 92:167-171. Medline
28. Majchrowicz E, Mendelson JH (1970) Blood concentrations of acetaldehyde and ethanol in chronic alcoholics. Science 168:1100-1102. CrossRef Medline
29. Manzanares J, Lookingland KJ, Moore KE (1991) Kappa opioid receptor-mediated regulation of dopaminergic neurons in the rat brain. J Pharmacol Exp Ther 256:500-505. Medline
30. McLaughlin JP, Li S, Valdez J, Chavkin TA, Chavkin C (2006) Social defeat stress-induced behavioral responses are mediated by the endogenous kappa opioid system. Neuropsychopharmacology 31:1241-1248. Medline
31. Mucha RF, Herz A (1985) Motivational properties of kappa and mu opioid receptor agonists studied with place and taste preference conditioning Psychopharmacology (Berl) 86:274-280. Medline
32. Ongür D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys, and humans. Cereb Cortex 10:206-219. CrossRef Medline
33. Pascoe JE, Williams KL, Mukhopadhyay P, Rice KC, Woods JH, Ko MC (2008) Effects of mu, kappa, and delta opioid receptor agonists on the function of hypothalamic-pituitary-adrenal axis in monkeys. Psycho neuroendocrinology 33:478-486. CrossRef Medline
34. Patel JC, Rice ME (2013) Monitoring axonal and somatodendritic dopamine release using fast-scan cyclic voltammetry in brain slices. Methods Mol Biol 964:243-273. CrossRef Medline
35. Paxinos G, Huang XF, Petrides M, Toga AW (2009) The rhesus monkey brain in stereotaxic coordinates, Ed 2. San Diego: Elsevier.
36. Pfeiffer A, Brantl V, Herz A, Emrich HM (1986) Psychotomimesis mediated by kappa opiate receptors. Science 233:774-776. CrossRef Medline
37. Porrino LJ, Lyons D, Smith HR, Daunais JB, Nader MA (2004) Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J Neurosci 24:3554-3562. CrossRef Medline
38. Saddoris MP, Sugam JA, Cacciapaglia F, Carelli RM (2013) Rapid dopamine dynamics in the accumbens core and shell: learning and action. Front Biosci 5:273-288. Medline
39. Schuckit MA, Anthenelli RM, Bucholz KK, Hesselbrock VM, Tipp J (1995) The time course of development of alcohol-related problems in men and women. J Stud Alcohol 56:218-225. Medline
40. Siciliano CA, Calipari ES, Ferris MJ, Jones SR (2014) Biphasic mechanisms of amphetamine action at the dopamine terminal. J Neurosci 34:5575-5582. CrossRef Medline
41. Siciliano CA, Calipari ES, Ferris MJ, Jones SR (2015) Adaptations of presynaptic dopamine terminals induced by psychostimulant self-administration. ACS Chem Neurosci 6:27-36. Medline
42. Sirohi S, Bakalkin G, Walker BM (2012) Alcohol-induced plasticity in the dynorphin/kappa-opioid receptor system. Front Mol Neurosci 5:95. Medline
43. Substance Abuse and Mental Health Services Administration (2012) National Survey on Drug Use and Health. http://www.samhsa. gov/data/NSDUH/2012SummNatFindDetTables/DetTabs/NSDUH-Det TabsSect2peTabs43to84-2012.htm#Tab2.71B.
44. Thompson AC, Zapata A, Justice JB Jr, Vaughan RA, Sharpe LG, Shippenberg TS (2000) Kappa-opioid receptor activation modifies dopamine uptake in the nucleus accumbens and opposes the effects of cocaine. J Neurosci 20:9333-9340. Medline
45. Vivian JA, Green HL, Young JE, Majerksy LS, Thomas BW, Shively CA, Tobin JR, Nader MA, Grant KA (2001) Induction and maintenance of ethanol self-administration in cynomolgus monkeys (Macaca fascicularis): longterm characterization of sex and individual differences. Alcohol Clin Exp Res 25:1087-1097. CrossRef Medline
46. Walker BM, Koob GF (2008) Pharmacological evidence for a motivational role of kappa-opioid systems in ethanol dependence. Neuropsychopharmacology 33:643-652. CrossRef Medline
47. Walker BM, Valdez GR, McLaughlin JP, Bakalkin G (2012) Targeting dynorphin/kappa opioid receptor systems to treat alcohol abuse and dependence. Alcohol 46:359-370. CrossRef Medline
48. Walker JM, Thompson LA, Frascella J, Friederich MW (1987) Opposite effects of mu and kappa opiates on the firing-rate of dopamine cells in the substantia nigra of the rat. Eur J Pharmacol 134:53-59. CrossRef Medline
49. Wanat MJ, Willuhn I, Clark JJ, Phillips PE (2009) Phasic dopamine release in appetitive behaviors and drug addiction. Curr Drug Abuse Rev 2:195-213. CrossRef Medline
50. Werling LL, Frattali A, Portoghese PS, Takemori AE, Cox BM (1988) Kappa receptor regulation of dopamine release from striatum and cortex of rats and guinea pigs. J Pharmacol Exp Ther 246:282-286. Medline
51. Yorgason JT, España RA, Jones SR (2011) Demon voltammetry and analysis software: analysis of cocaine-induced alterations in dopamine signaling using multiple kinetic measures. J Neurosci Methods 202:158-164. Medline