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Cardiovascular Function Is Altered by Picomole Injections of Glutamate Into Rat Medulla

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Cardiovascular Function Is Altered by Picomole Injections of Glutamate Into Rat Medulla The Journal of Neuroscience, May 1988, E(5): 1884-1693 Cardiovascular Function Is Altered by Picomole Injections of Glutamate into Rat Medulla D. 0. Nelson, Howard L. Cohen, Jack L. Feldman,” and Donald Ft. McCrimmon Departments of Physiology, Anesthesia, and Surgery, Northwestern University Medical School, Chicago, Illinois 60611 Local neural circuitry in the nucleus tractus solitarius (NTS) ferent paths provides the neuroanatomical substrate for inte- involved in cardiovascular control was studied by injecting gration and modulation of cardiovascular responses to mecha- nanoliter volumes of excitatory amino acids into the struc- noreceptor afferent signals. Thus, the NTS must function as ture. Experiments were performed on urethane-anesthe- more than a simple relay nucleus. tized, artificially ventilated rats. Multibarrel micropipettes The neuronal integration within the NTS requires informa- were used for pressure ejection of drugs or a dye for marking tion transfer between neurons in a complex network. The de- ejection sites. Ejected volumes, ranging from 200 pl to 25 tailed nuclear substructure and microanatomy of the NTS sug- nl, were directly monitored for every injection. Injections of gests that small aggregates of neurons may act as functional as little as 200 fmol of L-glutamate in 200 pl into the medial units. Yet, despite a growing body of neuroanatomical literature and lateral NTS region rostra1 to the obex elicited marked, indicating a complex substructure within the NTS (Kalia and site-specific .decreases in arterial pressure and heart rate. Mesulum, 1980; Paxinos and Watson, 1986; Kalia et al., 1984; The majority of these responses were eliminated by block- Kalia and Fuxe, 1985) this structure is often considered to ade of parasympathetic and sympathetic neural outflow. At possess fairly homogeneous function with respect to its role in sites caudal to obex, in the commissural region of the NTS, cardiovascular control. In this paper we describe an approach L-glutamate injections produced marked elevations in heart that indicates a functional heterogeneity in the NTS. Utilizing rate and arterial pressure which were sympathetically me- site-specific delivery of subpicomolar amounts of excitatory diated. Responses to L-glutamate were attenuated by con- amino acids in nanoliter volumes, we present evidence for a current injection of glutamic acid diethyl ester and oL-2-ami- complex regional organization underlying NTS integration and no-4-phosphonobutyrate, or lidocaine. These results indicate control of the circulation. a heterogeneity in the spatial organization of brain-stem cir- Materials and Methods cuitry underlying cardiovascular control that has not been previously described. Experiments were performed in 36 urethane(1 gm/kg)-anesthetizedrats weighing 300-400 gm. Polyethylenecatheters were insertedinto the left femoral artery and vein. The arterial catheterwas connectedvia a pres- The nucleus tractus solitarius (NTS) is the primary site of ter- sure transducer(Statham) to a polygraph for continuous recordingof mination of afferent nerve fibers arising from arterial and car- pulsatile and mean arterial pressures(MAP). Heart rate was determined diopulmonary mechanoreceptors (Crill and Reis, 1968; Murra by an integrating rate meter (Winston Electronics) driven by the lead II ECG signal. In some cases, tracheal cannulas were inserted and an- and Reis, 1969; Seller and Illert, 1969; Jordan and Spyer, 1977; imals paralyzed with gallamine trethiodide (1 mg/kg) and mechanically Ciriello and Calaresu, 198 1). Neurons in the NTS integrate these ventilated. The animals were placed in a stereotaxic frame with the head and other circulatory related afferent signals and are important inclined downward by 45”, and an occipital craniotomy was performed. in the production of appropriate patterns of cardiovascular, pul- The caudal portion of the fourth ventricle was exposed by incising the monary, and other homeostatic responses (Spyer, 198 1). Lesions dura and arachnoid and, when necessary, by gentle retraction of the cerebellum with a blunt glass probe. within this structure have far more severe influences than sino- Two- and three-barrel glass micropipettes were constructed with total aortic denervation on cardiovascular function. In the latter sit- tip diameters of 5-20 pm. Barrels contained 1 or 10 mM L-glutamate uation, arterial pressure shows only lability (Cowley et al., 1980) (Glu), a mixture of 100 mM glutamic acid diethyl ester (GDEE) and 10 compared with fulminating hypertension with pulmonary ede- mM DL-2-amino-4-phosphonobutyrate (APB), 4% lidocaine hydrochlo- ride, 2% pontamine sky blue, or 150 mM NaCl. Drugs were prepared ma and chronically maintained hypertension with the former in 150 mM NaCl and pH adjusted to 7.4 with 1 N NaOH; pontamine (Doba and Reis, 1973; Dejong and Palkovits, 1976; Talman et was prepared in 0.5 M sodium acetate. At closely spaced sites within al., 198 1). The rich innervation of the NTS by visceral afferents the NTS, measured volumes of drugs were injected with short-duration and numerous other CNS structures coupled with multiple ef- (10-500 msec)pressure (0.1-7.0 atmospheres)pulses. Ejectate volumes were measured directly by monitoring the movement of the fluid me- niscus in a pipette barrel with the aid of a 150 x compound microscope equipped with a fine reticule as described previously (McCrimmon et Received Aug. 22, 1986; revised Oct. 2, 1987; accepted Oct. 5, 1987. al., 1986). Direct monitoring of drug volume was imperative, as flow The technical assistance of Carol A. Graham and Marianne Otto is gratefully resistance of the electrode tip could change significantly following small acknowledged. This work was supported by NIH Grants HL29033 and NS-2 1036 and the Schweppe Foundation. (< 100 pm) displacements of the electrode. In experiments involving Correspondence should be addressed to Dr. Douglas 0. Nelson, Department electrical stimulation of the NTS region, one barrel of a multibarrel of Physiology, Northwestern University Medical School, 303 East Chicago Ave- micropipette was filled with 150 mM NaCl in 1% agar. For current nue, Chicago, IL 606 11. passage we used a silver-silver chloride wire inserted into the agar #Present address: Department of Kinesiology, University of California Los An- solution and connected to a constant-current stimulus isolation unit geles, 405 Hilgard Avenue, Los Angeles, CA 90024. connected to a stimulator. Current passed was calculated from the volt- Copyright o 1988 Society for Neuroscience 0270-6474/88/051684-10$02.00/O age drop across a series resistor in the ground path. The Journal of Neuroscience, May 1968, 8(5) 1665 Figure 1. Photomicrograph of a Nissl- counterstained coronal brain-stem sec- tion at low (A) and high (B) power il- lustrating a typical iontophoretically applied dye spot (arrow) marking the bottom of a penetration tract through the lateral aspect of the commissural region of the NTS. Scale bar, 400 pm (4) and 100 Frn (B). Mapping studies were carried out using 2- or 3-barrel micropipettes for possible nonspecific volume effects. At the site ofdeepest penetration containing 1 or 10 mM Glu, pontamine sky blue, and either saline or in an electrode tract, pontamine sky blue dye was iontophoretically an antagonist. The micropipette was positioned on the surface of the injected (20 @A DC for 10 min) to mark the injection site precisely. dorsal medulla and driven into the brain in 100-200 Frn steps. Pene- Using this protocol, we determined at selected sites (1) the dose (vol- tration tracks were referenced relative to the predetermined coordinates ume and concentration) dependence of blood pressure and heart rate of the obex and separated by 100-200 pm. A region extending from 1.5 responses, (2) the susceptibility of these responses to antagonism by mm rostra1 to 1 mm caudal to the obex, from midline to 1.2 mm laterial known excitatory amino acid receptor blocking agents, and (3) the region to midline, and from the dorsal medullary surface to approximately 1.4 from which a particular response was elicited, by dye injection and mm ventral was mapped. This region was chosen because it encom- histological reconstruction. In some animals, the effects of parasym- passes most of the NTS complex in which cardiovascular-related affer- pathetic blockade with atropine methyl nitrate (1.5 mg/kg, IV) followed ents are believed to terminate (Berger, 1979; Panneton and Loewy, by peripheral sympathetic blockade using phentolamine (1 mg/kg IV) 1980). At each site, 0.2-20 nl of Glu was injected, and the arterial on Glu-elicited depressor responses were measured. Similarly, m other pressure and heart rate responses were recorded on the polygraph and animals, the effects of administration of propranolol (0.5 mgkg, IV) analog tape. In subsequent experiments, additional electrode barrels followed by phentolamine and atropine methyl nitrate on Glu-elicited contained APB and GDEE or lidocaine. At each site, volumes of 150 pressor responses were examined. Receptor blockade of peripheral u-re- mM NaCl equal to the largest volume of Glu were injected to control ceptors was tested by intravenous administration of phenylephrine (100 1666 Nelson et al. * Effects of Glutamate on Cardiovascular Control Figure 2. Dose-dependent decreases in arterial pressure and heart rate pro- duced by injections of Glu at a single site in the NTS. A, Reconstruction of injection site (dot) located approxi- mately 1100 pm rostra1 to obex in the medial NTS and 750 pm below the brain surface. B. Heart rate (HR. born) and arterial pressure (BP, mm figj re: sponses to nanoliter injections of 10 mM Glu. Arrows and numbers below arrows indicate time and volume (in nanoli- ters) of injections. Note the rapid-onset decrease in arterial pressure, but not heart rate, which occurred with 250 pl (2.5 pmol) of Glu. C, Dose-response curve depicting decreases in arterial pressure and heart rate as a function of Glu injection volume for this site. Threshbld of the heart rate response was aooroximatelv__ .
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