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Stimulation of Endorphin Neurotransmission in the Nucleus Accumbens by Ethanol, Cocaine, and Amphetamine

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Stimulation of Endorphin Neurotransmission in the Nucleus Accumbens by Ethanol, Cocaine, and Amphetamine The Journal of Neuroscience, 2001, Vol. 21 RC184 1of5 Stimulation of Endorphin Neurotransmission in the Nucleus Accumbens by Ethanol, Cocaine, and Amphetamine M. Foster Olive,1 Heather N. Koenig,1 Michelle A. Nannini,1 and Clyde W. Hodge2 1Department of Neurology and Ernest Gallo Clinic and Research Center, University of California at San Francisco, Emeryville, California 94608, and 2Center for Alcohol Studies, School of Medicine, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599 Numerous studies have demonstrated that drugs of abuse ministered intraperitoneally twice at 3 h intervals, and the en- activate the mesolimbic dopamine reward pathway, and it is dorphin content of microdialysates was analyzed by a solid- widely held that this activation contributes to the motivational phase radioimmunoassay. Acute administration of ethanol, and positive reinforcing properties of these substances. How- cocaine, and D-amphetamine transiently elevated extracellular ever, there is evidence that endogenous opioid systems within levels of endorphins in the nucleus accumbens, whereas nico- this brain reward circuit also play a role in drug reinforcement tine and saline were without effect. We hypothesize that this and drug-seeking behavior. Using microdialysis in freely moving drug-induced release of endorphins may contribute to the pos- rats, we sought to determine whether various drugs of abuse itive reinforcing and motivating properties of ethanol and (i.e., ethanol, cocaine, D-amphetamine, and nicotine) would psychostimulants. increase neurotransmission of endogenous opioid peptides Key words: microdialysis; endorphin; cocaine; ethanol; am- (i.e., endorphins) in the nucleus accumbens. Drugs were ad- phetamine; nicotine; addiction The most well-characterized change in brain neurochemistry underlying drug reward and positive reinforcement. The present caused by drugs of abuse is an increase in extracellular dopamine study was conducted to assess the ability of certain drugs of abuse levels in the nucleus accumbens (NAc) of the basal forebrain, and (i.e., ethanol, cocaine, amphetamine, and nicotine) to alter extra- many lines of evidence suggest that this increase in dopamine cellular levels of endogenous opioid ligands (endorphins) in the release plays a role in the rewarding and positive reinforcing NAc using microdialysis sampling in freely moving animals. effects of drugs of abuse (for review, see Koob, 1992; Wise, 1998; Spanagel and Weiss, 1999). However, it has long been suspected MATERIALS AND METHODS that endogenous opioid peptides such as endorphins also play a Animals. Male Long–Evans rats (250–400 gm, 10–20 weeks of age; Harlan, Madison, WI) were used as subjects. Animals were housed role in drug reward, in positive reinforcement, and ultimately in individually under a 12 hr light/dark cycle with lights on at 6:00 A.M. the development of addiction. For example, early studies demon- Before surgical procedures, animals were housed in standard Plexiglas strated that endogenous ligands of ␮ and ␦ opioid receptors, such cages maintained at 25°C in a ventilated cage rack (Biozone Inc., Fort as enkephalins and endorphins, possess intrinsic rewarding prop- Mill, SC). After surgical procedures, animals were housed in clear ϫ erties and will be self-administered by rodents directly into the cylindrical polycarbonate microdialysis cages (30 cm diameter 38 cm high; Instech Laboratories, Plymouth Meeting, PA) for the remainder of brain ventricles (Belluzzi and Stein, 1977; van Ree et al., 1979) as the experiments. Animals had access to food and water ad libitum well as regions of the mesolimbic reward system such as the NAc throughout all procedures. All experiments were performed during the (Goeders et al., 1984). Along these lines, intracranial microinjec- light portion of the light/dark cycle. All procedures were performed in tions of enkephalins, endorphins, and other ␮/␦ receptor agonists accordance with approved institutional protocols, the 1996 National Research Council Guide for the Care and Use and Laboratory Animals, and the NAc and other regions can produce conditioned place pref- the Society for Neuroscience Policy on the Use of Animals in Neuroscience erence, a behavioral measure of reward and positive reinforce- Research. ment (Olds, 1982; van der Kooy et al., 1982; Bals-Kubik et al., Surgical procedures. Animals were anesthetized with 2% halothane 1993). Finally, administration of ␮ and/or ␦ opioid receptor vaporized in a 1:1 mixture of O2 and N2O and implanted with guide antagonists into the NAc can reduce appetitive behaviors and cannulas (SciPro, North Tonawanda, NY) aimed at the medial border of self-administration of certain drugs of abuse (Amalric et al., 1987; Corrigall and Vaccarino, 1988; Kelley et al., 1996; Heyser et al., 1999; Hyytia and Kiianmaa, 2001). Thus, ␮/␦ opioid receptors in This article is published in The Journal of Neuroscience, Rapid the NAc appear to be involved in the neurobiological mechanisms Communications Section, which publishes brief, peer- reviewed papers online, not in print. Rapid Communications Received July 10, 2001; revised Sept. 5, 2001; accepted Sept. 12, 2001. are posted online approximately one month earlier than they This research was supported by funds from the State of California for medical research on alcohol and substance abuse through the University of California at San would appear if printed. They are listed in the Table of Francisco. We thank Hoa Lam and Nigel Maidment for technical advice on radio- Contents of the next open issue of JNeurosci. Cite this article immunoassay procedures. as: JNeurosci, 2001, 21:RC184 (1–5). The publication date is Correspondence should be addressed to Dr. M. Foster Olive, Department of Neurology/Gallo Center, University of California at San Francisco, 5858 Horton the date of posting online at www.jneurosci.org. Street, Suite 200, Emeryville, CA 94608. E-mail: [email protected]. Copyright © 2001 Society for Neuroscience 0270-6474/01/210001-06$15.00/0 http://www.jneurosci.org/cgi/content/full/5844 2of5 J. Neurosci., 2001, Vol. 21 Olive et al. • Ethanol, Psychostimulants, and Endorphin Release the core–shell region of the NAc [stereotaxic coordinates: anteroposte- rior, ϩ1.7 mm; mediolateral, Ϫ1.0 mm from bregma; dorsoventral, Ϫ6.0 mm from skull surface, according to the atlas of Paxinos and Watson (1997)]. Guide cannulas were secured with skull screws and dental cement. The wound was treated with 2% bacitracin and 2% xylocaine topical ointments and sutured closed with 3-0 vicryl sutures. After surgery, animals were allowed to recover in polycarbonate microdialysis cages for at least 5 d before dialysis probe implantation. Microdialysis procedures. After recovery, animals were lightly reanes- thetized as described above and implanted with microdialysis probes with 2 mm polyethylsulfone membranes (15 kDa cutoff; 0.6 mm outer diameter; SciPro) to a final depth of Ϫ8.0 mm from skull surface. Probes were continuously perfused with artificial CSF (aCSF) containing 125 ⅐ mM NaCl, 2.5 mM KCl, 0.5 mM NaH2PO4 H2O,5mM Na2HPO4,1mM ⅐ ⅐ MgCl2 6H2O, 1.2 mM CaCl2 2H2O,5mMD-glucose, 0.2 mML-ascorbic acid, and 0.025% (w/v) bovine serum albumin, pH 7.3–7.5. All aCSF reagents were from Sigma (St. Louis, MO). Probes were attached to dual-channel liquid swivels (Instech Laboratories) with fluoroethylene polypropylene tubing (0.005 inch inner diameter; CMA/Microdialysis, North Chelmsford, MA) in cylindrical microdialysis cages to permit freely moving conditions. Animals were allowed to recover from probe implantation overnight before pharmacological experiments. On the fol- lowing day, the aCSF flow rate was set at 2.0 ␮l/min,andaftera1h re-equilibration period, microdialysis samples were collected into polypropylene microcentrifuge tubes in a refrigerated microsampler (SciPro) at 30 min intervals. After collection, samples were immediately stored on dry ice and later frozen at Ϫ70°C until analysis by radioimmu- noassay (RIA). Brain histology. After microdialysis procedures, animals were deeply anesthetized with Nembutal (150 mg/kg, i.p.) and perfused transcardi- ally with 100 ml of 0.9% NaCl followed by 250 ml of Streck tissue fixative (Streck Laboratories, La Vista, NE). Brains were then removed and placed in the same fixative for at least 48 h at 4°C. Coronal brain sections (30 ␮m thickness) were cut on a cryostat (Leica, Deerfield, IL), mounted onto microscope slides, and coverslipped with Permount (Fisher Scien- tific, Santa Clara, CA). Probe placement was verified under light micros- copy, and data from animals with probe placements outside of the target region were discarded. Figure 1. Diagram of coronal sections of rat brain indicating the location Endorphin RIA. Microdialysate endorphin content was measured us- of dialysis probe placements along the medial core–shell border of the ing a commercially available RIA kit (RK-022-33; Phoenix Pharmaceu- NAc. Vertical lines indicate the approximate location of the probe mem- ticals, Mountain View, CA) adapted to solid-phase procedures (Olive brane derived from histological sections. Numbers indicate anterior dis- and Hodge, 2001). Briefly, 96-well microtiter plates (Dynex Microlite 2ϩ; tance (in millimeters) from bregma (B). This figure was adapted from Dynex Technologies, Chantilly, VA) were incubated with a protein A Paxinos and Watson (1997). ␮ ␮ solution (0.4 g/50 lin0.1M NaHCO3, pH 9.0) for at least 24 h at 4°C to facilitate binding of the antisera to the plate wells. Plates were then Next, for each animal, dialysate endorphin content was transformed into washed three times with assay buffer [0.15 M K2HPO4, 0.2 mM ascorbic a percentage of basal endorphin release, assigning a value of 100% to the acid, 0.1% Tween 20, and 0.1% gelatin (Sigma), pH 7.4, with phenol red average endorphin level in the six 30 min baseline samples collected added for enhanced visualization]. Next, plates were incubated with Ϯ ␤ ␮ before drug administration. All data are presented as mean SEM. rabbit antisera to rat -endorphin (50 l/well; diluted 1:25 from stock in Individual postinjection data points were compared with baseline values assay buffer) for 24 h at 4°C.
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