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Cervical Sympathetic Trunk Proc. Natl. Acad. Sci. USA Vol. 80, pp. 4179-4183, July 1983 Neurobiology Frequency-dependent activation of glucose utilization in the superior cervical ganglion by electrical stimulation of cervical sympathetic trunk (deoxy['4C]glucose/energy metabolism) PAUL YAROWSKY*, MASSAKO KADEKARO, AND LOUIS SOKOLOFF' Laboratory of Cerebral Metabolism, National Institute of Mental Health, U.S. Public Health Service, Department of Health and Human Services, Bethesda, Marvland 20205 Contributed by Louis Sokoloff, April 15, 1983 ABSTRACT Electrical stimulation of the distal stump of the at least to the point of saturation (3, 6). These results raise the transected cervical sympathetic trunk produces a frequency-de- question of the mechanism of the coupling between functional pendent activation of glucose utilization, measured by the de- and metabolic activities. Presumablv the metabolic activation oxy['4C]glucose method, in the superior cervical ganglion of the in the structures of the brain is elicited, or at least initiated, by urethane-anesthetized rat. The frequency dependence falls be- electrical signals transmitted from the stimulated retina to its tween 0-15 Hz; at 20 Hz the activation of glucose utilization is no projection areas. greater than at 15 Hz. Deafferentation of the superior cervical The present studies were carried out to examine the influ- ganglion by transection of the cervical sympathetic trunk does not ence of electrical activity in an afferent pathway on the rate of diminish the rate of glucose utilization in the ganglion in the ure- utilization of the neural structure innervated bv it. thane-anesthetized rat. These results indicate that the rate of glucose energy metabolism in an innervated neural structure is, at least Specifically, the influence of spike frequency was examined. in part, regulated by the impulse frequency of the electrical input The experiments were carried out on the superior cervical gan- to the structure, and this regulation may be an essential compo- glion of the urethane-anesthetized rat because of the ease with nent of the mechanism of the coupling of metabolic activity to which the afferent nerves to this structure can be identified, functional activity in the nervous system. isolated, and electrically stimulated and the physiological ac- tivation of the ganglion monitored in the target organs inner- The autoradiographic deoxyglucose method was designed to vated by its efferent nerves. The results demonstrate a fre- measure the rates of glucose utilization simultaneously in all of quency-dependent activation of glucose utilization in the superior the anatomical and functional components of the nervous sys- cervical ganglion by electrical stimulation of the cervical sym- tem in conscious animals (1). Its use has demonstrated a close pathetic trunk in the physiological range of spike frequency in relationship between local functional activity and glucose uti- this neural system. lization in nervous tissue (2), and it has been extensively ap- plied to identify structures in the nervous system with altered MATERIALS AND METHODS functional activity in experimentally induced physiological, Chemicals. 2-Deoxy-D-[1-'4C]glucose (specific activity = 50- pharmacological, and pathophysiological states (2-4). Its use as 55 mCi/mmol; 1 Ci = 3.7 x 10'° Bq) was purchased from New a tool to map functional neural pathways is based on the prin- England Nuclear. Calibrated ["4C]toluene, used for internal ciple of an evoked metabolic response. Conditions that increase standardization in the measurement of plasma deoxy['4C]glu- the functional activitv of a neural structure lead to an enhance- cose concentrations, was also obtained from New England Nu- ment of its rate of glucose utilization; decreased functional ac- clear. tivity depresses this rate. An essential feature of the deoxyglu- Animals. Normal adult male Sprague-Dawley rats were pur- cose method is its use of quantitative autoradiography to localize chased from Taconic Farms (Germantown, NY). The experi- the rates of glucose utilization to specific structures in the ner- ments were carried out on animals weighing 270-430 g. The vous system (1). The metabolic effects of altered functional ac- animals were allowed water ad lib but were fasted for 15-18 hr tivity are often so pronounced that the direction and location prior to the experiment. of the changes in metabolic rate can be directly visualized in Preparation of the Animals. The surgical preparation of the the autoradiographs (2-4). animals and the experiments were carried out under urethane Studies in sensory systems, particularly the visual system, anesthesia. Urethane was chosen as the anesthetic agent to have demonstrated a quantitative relationship between the minimize the possibility of blockade of ganglionic transmission functional activity and the rate of glucose utilization in the neural by the anesthesia (7). The animals were anesthesized by the tissues. In the rat the rate of glucose utilization in the regions intraperitoneal injection of 1 g of urethane per kg of body weight. of the brain to which the retina projects is linearly related to Catheters were inserted into one femoral artery and vein, and the frequency of retinal stimulation by light flashes (5). In the the superior cervical ganglia and cervical sympathetic trunks dark-adapted rat the rates of glucose utilization in the super- were exposed bilaterally. Anesthesia was subsequently main- ficial layer of the superior colliculus and the lateral geniculate tained by the intermittent administration of urethane via the nucleus are directly proportional to the logarithm of the inten- venous catheter as needed. The cervical sympathetic trunks sity of retinal illumination by randomly spaced flashes of light, *Present address: Dept. of Pharmacology and Experimental Thera- The publication costs of this article were defrayed in part by page charge peutics, Univ. of Maryland School of Medicine, 660 WV. Redwood St., payment. This article must therefore be hereby marked "advertise- Baltimore, MD 21201. ment" in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 4179 Downloaded by guest on October 1, 2021 4180 Neurobiology: Yarowsky et al. Proc. Natl. Acad. Sci. USA 80 (1983) were dissected free from the common carotid arteries and the zation in the superior cervical ganglion were initiated approx- vagus nerves. In 33 animals in which the effects of electrical imately ll/2 hr in one series or 3-4 hr in the other series after stimulation of the afferent pathway were examined, the cervi- the onset of the urethane anesthesia. The two periods of anes- cal sympathetic trunk on both sides was transected about 1 cm thesia were examined separately because it has been found by from the caudal pole of the superior cervical ganglion, and a Ito et al. (10) that urethane causes a transient stimulation of glu- small segment of the nerve was removed. Transection of the cose utilization in the superior cervical ganglion, probably in- cervical trunk at this distance from the ganglion does not dis- directly via adrenomedullary mechanisms, which disappears after turb the blood supply to the ganglion (8). In 11 animals used a period of time (unpublished data). as controls to determine the effects of deafferentation per se, Physiological Status. The physiological status of the animals the cervical sympathetic trunks were similarly exposed bilat- was monitored during the experimental period by measure- erally but transected on only one side with the other left intact. ment of mean arterial blood pressure and arterial pCO2, pH, Electrical Stimulation. The distal portion of one transected and P02. Body temperature was maintained at 370C by means cervical sympathetic trunk was placed on bipolar platinum elec- of an electric heating pad. trodes in a mineral oil bath and stimulated via a stimulus iso- lation unit with pulses of 0.5 msec in duration at a current in- RESULTS tensity of 250 AA and at a frequency of 5, 10, 15, or 20 Hz. The current intensity was measured with an analog milliammeter Physiological Variables. Blood pH, pCO2, and P02 were (Hewlett-Packard model 428B). The stimulating cathode was maintained within normal levels during the urethane anes- positioned proximal to the ganglion. The effectiveness of the thesia. However, at the doses used, urethane caused a marked electrical stimulation was monitored by observation of the fall in mean arterial blood pressure from a normal mean level physiological responses in the ipsilateral eye-i.e., mydriasis, of approximately 130 mm of Hg to 80 mm of Hg and a moderate exophthalmos, and widening of the palpebral fissure. The elec- bradycardia from a normal mean heart rate of 482 to one of 342 trical stimulation was begun 5 min before the onset of the pe- beats per min. The changes in cardiovascular variables were riod of measurement of glucose utilization and was continued sustained throughout the experimental period. until approximately 5 min before the termination of the mea- Effects of Deafferentation on Glucose Utilization of Su- surement. perior Cervical Ganglion. The rate of glucose utilization in the Measurement of Glucose Utilization. The period of mea- superior cervical ganglion of the normal conscious rat is ap- surement of glucose utilization was initiated by the intravenous proximately 20 Amol/100 g per min (10). Urethane anesthesia this is administration of a pulse of 125 ACi of deoxy['4C]glucose (spe- stimulates rate, but the stimulation
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