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Regional Cerebral Glucose Utilization During Morphine Withdrawal in the Rat (Cerebral Metabolism/Limbic System/Drug Dependence) G

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Regional Cerebral Glucose Utilization During Morphine Withdrawal in the Rat (Cerebral Metabolism/Limbic System/Drug Dependence) G Proc. Natl Acad. Sci. USA Vol. 79, pp. 3360-3364, May 1982 Neurobiology Regional cerebral glucose utilization during morphine withdrawal in the rat (cerebral metabolism/limbic system/drug dependence) G. F. WOOTEN, P. DISTEFANO, AND R. C. COLLINS Departments of Neurology and Pharmacology, Division of Clinical Neuropharmacology, Washington University School of Medicine, St. Louis, Missouri 63110 Communicated by Oliver H. Lowry, February 26, 1982 ABSTRACT Regional cerebral glucose utilization was studied precipitated morphine withdrawal in the rat. A preliminary re- by 2-deoxy['4C]glucose autoradiography in morphine-dependent port of this work has appeared as an abstract (17). rats and during naloxone-induced morphine withdrawal. In mor- phine-dependent rats, glucose utilization was increased compared MATERIALS AND METHODS with naive controls uniformly (23-54%) in hippocampus, dentate gyrus, and subiculum and reduced in frontal cortex, striatum, an- Preparation of Animals. Male Sprague-Dawley rats weigh- terior ventral thalamus, and medial habenular nucleus. On pre- ing 275-325 g were used. On experimental day 1, a single pellet cipitation ofmorphine withdrawal by subcutaneous administration containing 75 mg of morphine as free base was implanted sub- of naloxone at 0.5 mg/kg to morphine-dependent rats, glucose cutaneously under light ether anesthesia. On day 4, two pellets, utilization was increased in the central nucleus ofamygdala (51%), each containing 75 mg of morphine as free base, were im- lateral mammillary nucleus (40%), lateral habenular nucleus planted. On day 7, after being deprived of food for 12 hr, the (39%), medial mammillary nucleus (35%), and medial septal nu- rats were lightly anesthetized with 2% halothane, the pellets cleus (35%) (all, P < 0.01). Significant increases also occurred in were removed, and a polyethylene cannula was implanted into several other limbic structures including interpeduncular nucleus, the right externaljugular vein for subsequent injections. At least anterior medial and ventral thalamic nuclei, and lateral septal 2 hr of recovery time was allowed before injection of naloxone nucleus. Knowledge of the functional cerebral anatomy of the at 0.5 mg/kg subcutaneously to induce morphine withdrawal. morphine-withdrawal syndrome should facilitate studies directed Controls consisted of naive rats (n = 5), rats made dependent toward understanding the molecular mechanisms of opiate on morphine but injected on day 7 with normal saline rather withdrawal. than naloxone (morphine dependent; n = 4), and naive rats re- ceiving naloxone at 0.5 mg/kg subcutaneously (n = 3). Five rats Abrupt termination of chronic morphine treatment or admin- were studied during naloxone-induced morphine withdrawal. istration of opiate antagonists to morphine-dependent animals 2-Deoxy['4C]glucose Autoradiography. 2-Deoxy['4C]glucose results in a complex withdrawal syndrome composed of both autoradiography was carried out according to the method of stereotyped behavioral and autonomic features (1, 2). The be- Sokoloff et aL (8). Ten minutes after subcutaneous injection of havioral concomitants of morphine withdrawal in rodents in- naloxone at 0.5 mg/kg or normal saline, 2 deoxy['4C]glucose clude wet dog shakes, jumping or escape attempts, teeth chat- (25 ,uCi per rat; 1 Ci = 3.7 X 10"' becquerels) was injected into tering, and abnormal posturing; autonomic features include the awake freely moving rats via the venous cannula. Forty-five diarrhea, weight loss, hypothermia, seminal emissions, and minutes later, the animals were killed with intravenous sodium ptosis. Although much information has accumulated in recent pentobarbital and perfused with 0.2 M sodium cacodylate (pH years regarding the identity and distribution of endogenous 7.3) and then with 3.3% paraformaldehyde in the same buffer. opiates (3, 4) and their receptor sites (5, 6) in the central nervous The brain was removed, rapidly frozen in liquid Freon, and system, there is little knowledge of those areas of the central mounted on brass chucks. Duplicate 20-lim sections were taken nervous system critical for expression of the morphine-with- every 200 Aum, mounted on cover glasses, and exposed to Kodak drawal syndrome (7). SB-5 x-ray film for exactly 5 days. Selected sections were then The 2-deoxyglucose autoradiographic method of Sokoloff et taken for thionin staining and densitometry was carried out on aL (8) has been ofgreat utility in characterizing functional cere- the autoradiographs. OD results are expressed as OD ofa given bral anatomy. The physiological activity of neurons requires region/OD of the corpus callosum ratios. Mean blood glucose energy derived from the metabolism of glucose. By mapping levels (mg/ml; ± SD) during naloxone-precipitated morphine regional cerebral glucose utilization, inferences can be made withdrawal were 1.87 ± 0.57; levels in naive rats treated acutely about regional physiological neuronal activity. The method has with naloxone were 1.15 ± 0.23 and those in morphine-depen- been used to study a variety ofexperimental paradigms includ- dent rats treated acutely with normal saline were 1.66 ± 0.10. ing the routes ofcentral processing ofperipheral sensory stimuli Therefore, changes in endogenous blood glucose levels were (9, 10), the spread offocal seizure activity (11, 12), central sites not likely to independently alter the autoradiographic images ofdrug action (13, 14), and the consequences ofrestricted brain in rats during naloxone-precipitated morphine withdrawal. lesions (15, 16). In an attempt to characterize the functional Student's t test was used to determine the significance ofthe cerebral anatomy of morphine withdrawal, we have used the differences in glucose utilization between various treatment 2-deoxyglucose autoradiographic method to describe relative groups (18). regional cerebral rates of glucose utilization during naloxone- RESULTS The publication costs ofthis article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertise- Morphine-dependent rats that received naloxone at 0.5 mg/ ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. kg subcutaneously on day 7 rapidly developed a morphine-with- 3360 Downloaded by guest on September 24, 2021 Neurobiology: Wooten et al. Proc. Natl. Acad. Sci. USA 79 (1982) 3361 drawal syndrome consisting of tachypnea, increased motor ac- had no overt behavioral changes. tivity, wet dog shakes, and diarrhea. The animals vocalized Regional brain glucose utilization in naive controls, in mor- when handled but did not exhibit the "jumping" and "flying" phine-dependent rats, and in rats during naloxone-induced phenomena, behaviors that are thought to be environmentally morphine withdrawal is summarized in Table 1. Increased glu- determined. In contrast, morphine-dependent rats that re- cose utilization relative to naive controls in morphine-depen- ceived normal saline subcutaneously on day 7 remained quiet dent rats not given naloxone was found in the medial, lateral, and alert, exhibiting no apparent abnormal behavior. Likewise, and magnocellular preoptic areas, bed nucleus of the stria ter- naive rats treated with naloxone at 0.5 mg/kg subcutaneously minalis, parasubiculum, subiculum, medial and lateral entorhi- Table 1. 2-Deoxy[14C]glucose incorporation into brain regions in morphine-dependent and -withdrawing rats Morphine dependent Morphine withdrawal Brain region Naive control (n = 5) (n = 4) (n = 5) Cortex Frontal motor 3.41 ± 0.19 2.80 ± 0.15 3.00 ± 0.49 Medial frontal 3.72 ± 0.22 3.30 ± 0.16 3.21 ± 0.44 Cingulate gyrus 3.46 ± 0.31 3.31 ± 0.33 3.33 ± 0.13 Pyriform 2.30 ± 0.13 2.39 ± 0.16 2.58 ± 0.20 Orbital frontal 4.28 ± 0.22 3.74 ± 0.62 4.12 ± 0.39 Basal ganglia Striatum 3.56 ± 0.36 2.94 ± 0.26 3.09 ± 0.21 Globus pallidus 2.17 ± 0.13 1.96 ± 0.13 2.00 ± 0.17 Substantia nigra (P.C.) 2.49 ± 0.43 2.28 ± 0.16 2.61 ± 0.21 Substantia nigra (P.R.) 1.83 ± 0.36 1.80 ± 0.04 2.09 ± 0.34 Subthalamic nucleus 3.11 ± 0.13 2.99 ± 0.20 3.15 0.35 Thalamus Paratenial nucleus 2.77 ± 0.26 2.94 ± 0.17 3.67 ± 0.31 T T Anterior ventral nucleus 3.72 ± 0.23 3.13 0.25 4.08 ± 0.50 t Anterior medial nucleus 3.25 ± 0.28 2.87 ± 0.24 3.73 ± 0.23 T T Preoptic area Medial preoptic area 1.49 ± 0.25 2.11 ± 0.22 T T 1.98 ± 0.33 Lateral preoptic area 1.61 ± 0.12 2.24 ± 0.30 T T 2.02 ± 0.21 Bed nucleus stria terminalis 1.74 ± 0.21 2.28 0.24 t 2.70 ± 0.24 T Preoptic magnocellularis 1.99 ± 0.32 3.07 ± 0.44 T 3.06 ± 0.29 "Limbic system" Amygdala-central nucleus 2.72 ± 0.25 2.55 ± 0.28 3.85 ± 0.34 T T T Amygdala-medial nucleus 1.76 ± 0.15 1.61 ± 0.07 2.18 ± 0.34 T T Amygdala-basolateral nucleus 2.09 ± 0.16 2.09 ± 0.15 2.28 ± 0.17 Medial septal nucleus 2.43 ± 0.21 2.30 ± 0.13 3.10 ± 0.26 1 1 Lateral septal nucleus 2.06 ± 0.23 2.02 ± 0.11 2.54 ± 0.24 T t Medial habenular nucleus 3.27 ± 0.47 2.44 ± 0.30 2.81 ± 0.21 Lateral habenular nucleus 4.08 ± 0.26 3.64 ± 0.53 5.25 ± 0.78 T Medial mammillary nucleus 3.89 ± 0.44 3.41 ± 0.58 4.70 ± 0.43 T Lateral mammillary nucleus 3.89 ± 0.54 3.41 ± 0.60 4.77 ± 0.47 t Interpeduncular nucleus 3.80 ± 0.38 3.67 ± 0.34 4.69 ± 0.50 T Nucleus accumbens 2.86 ± 0.27 2.51 ± 0.23 2.93 ± 0.18 T Dorsal presubiculum 2.92 ± 0.32 3.28 ± 0.10 3.28 ± 0.73 Parasubiculum 2.23 ± 0.28 3.02 ± 0.10 T T T 2.60 ± 0.55 Subiculum 2.21 ± 0.29 3.03 ± 0.04 T T 2.36 ± 0.40 Medial entorhinal cortex 1.82 ± 0.16 2.85 ± 0.25 T T T 2.00 ± 0.34 Lateral entorhinal cortex 1.85 ± 0.35 2.69 ± 0.13 TT 1.94 ± 0.36 Dorsal hippocampus CA-1 pyramidal layer 1.56 ± 0.12 1.96 ± 0.26 T 1.77 ± 0.18 CA-1 stratum radiatum 1.58 ± 0.14 2.18 ± 0.34 T T 1.71 ± 0.16 Perforant path 2.23 ± 0.25 2.98 ± 0.23 1T 2.60 ± 0.39 Dentate gyrus 1.43 ± 0.11 2.21 ± 0.20 T 1 T 1.97 ± 0.18 CA-3 pyramidal layer 1.80 ± 0.14 2.27 ± 0.23 T t 1.94 0.10 "CA-2" 2.08 ± 0.34 2.57 ± 0.26 T 2.28 ± 0.24 Ventral hippocampus CA-1 pyramidal layer 1.80 ± 0.31 2.46 ± 0.42 1 2.17 ± 0.22 CA-1 stratum radiatum 1.75 ± 0.34 2.37 ± 0.38 T 1.90 ± 0.21 Perforant path 2.56 ± 0.45 3.31 ± 0.24 1 T 2.76 ± 0.58 Dentate gyrus 1.78 ± 0.45 2.53 ± 0.34 T 2.22 ± 0.42 Ventral subiculum 1.79 ± 0.42 2.50 ± 0.56 2.34 ± 0.38 Results represent mean ± SD of the OD of the region in question/OD of the corpus callosum ratio.
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