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A Circumscribed Projection from the Nucleus of the Solitary Tract to The

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The Journal of Neuroscience, May 1989, g(5): 1668-l 682 A Circumscribed Projection from the Nucleus of the Solitary Tract to the Nucleus Ambiguus in the Rat: Anatomical Evidence for Somatostatin-284mmunoreactive Interneurons Subserving Reflex Control of Esophageal Motility E. T. Cunningham, Jr.‘s21a and P. E. Sawchenko2 ‘Department of Neurosciences, University of California, San Diego, La Jolla, California 92093, and 2The Salk Institute for Biological Studies and The Clayton Foundation for Research-California Division, La Jolla, California 92037 Axonal transport and immunohistochemical methods were The nucleus of the solitary tract (NTS) occupies a pivotal po- used to investigate the anatomical and biochemical orga- sition in the central visceromotor system. Projections of the nization of projections from the nucleus of the solitary tract Vth, VIIth, IXth, and Xth cranial nerves terminate centrally (NTS) to the rostral, esophageal, part of the nucleus ambig- within the NTS, conveying sensoryinformation from the oral, uus (NA) in the rat. Discrete iontophoretic deposits of a ret- thoracic, and abdominal cavities. The NTS, in turn, projects to rogradely transported tracer, fluorogold, placed in the rostra1 virtually all levels of the neuraxis, so as to coordinate appro- NA labeled a column of cells within the NTS, termed the priate behavioral, neuroendocrine, and autonomic responses central part of the NTS (after Ross et al., 1985) situated just (seeSawchenko, 1983; Norgren, 1984, for reviews). medial to the solitary tract and extending from about 300 to Prominent among the projections of the NTS is an input to 1000 pm rostra1 to the obex. lontophoretic deposits of the the ventrolateral medulla (Morest, 1967; Cottle and Calaresu, anterogradely transported tracer, Phaseohs vulgaris-leu- 1975; Palkovits and Zaborszky, 1977; Loewy and Burton, 1978; coagglutinin (PHA-L), placed in the central part of the NTS Norgren, 1978; Ricardo and Koh, 1978; Becksteadet al., 1980; gave rise to dense and topographically restricted projections Sawchenkoand Swanson, 1982; Bieger, 1984; Stuesseand Fish, to the rostra1 NA. More caudal and ventral aspects of the NA 1984; Ross et al., 1985; Lovick, 1986; Dampney et al., 1987; did not receive prominent inputs from the central part of the Blessinget al., 1987) a region whose best-characterizedoutput NTS, and deposits that spared the central part of the NTS neurons include catecholaminergic neurons of the Al and Cl gave rise to only sparse projections to the rostra1 NA. Anti- cell groups and motor neurons of the vagus and glossopha- sera against somatostatin-28 (SS-28) stained cell bodies ryngeal nerves. Current evidence suggeststhat the catechol- within the central part of the NTS. In addition, a double- aminergic cell groups play distinctive roles in autonomic and/ labeling procedure, capable of colocalizing anterogradely or neuroendocrine controls of stress-and cardiovascular-related transported PHA-L and endogenous peptides to individual responses(Ross et al., 1981, 1983, 1984; Sawchenkoand Swan- fibers and/or terminals, demonstrated an appreciable num- son, 1982; Cunningham and Sawchenko, 1987, 1988; Morrison ber of SS-284mmunoreactive terminals within the rostra1 NA et al., 1988; seeCiriello et al., 1986, and Reis, 1988, for reviews). that arose from the NTS. Correspondingly, unilateral lesions By contrast, the function of vagal and glossopharyngealmotor that involved the central part of the NTS resulted in a marked neurons in the ventrolateral medulla has remained a topic of depletion of SS-28 immunoreactivity in the ipsilateral rostra1 debate, due primarily to conflicting data concerning the repre- NA. These data provide evidence for a discrete, partly so- sentation of the various viscera in the ambigual complex (see matostatinergic, projection from the central part of the NTS Bieger and Hopkins, 1987, for review). The selectivity, in terms to the rostra1 NA. Anatomical and physiological studies im- of the distribution, cells of origin, and chemical coding, of NTS plicating the central part of the NTS and the rostra1 NA in projections to each of these individual cell groups has not yet esophageal function suggest this pathway to be involved in been deciphered.The present study representsan initial attempt the reflex control of esophageal motility. to evaluate the specificity of projections from the NTS to the ventrolateral medulla, focusing first on inputs to the nucleus ambiguus (NA). Received Aug. 22, 1988; revised Oct. 17, 1988; accepted Oct. 18, 1988. Recently, Bieger and Hopkins (1987) employed retrograde Supported by NIH Grant HL-35 137, a M&night Foundation Scholar’s award tracing techniques to addressthe issueof viscerotopy within the (P.E.S.) and by a Grant-in-Aid of Research from Sigma Xi (E.T.C., Jr.). This work nucleus ambiguus(NA). Their results, in agreementwith many was conducted in part by the Clayton Foundation for Research-California Di- vision; P.E.S. is a Clayton Foundation Investiaator. We thank R. Benoit for of the degeneration studiesdone at the turn of the century (see generously providing antisera to somatostatin, anh R. Benoit and L. W. Swanson Molhant, 1914, and Lawn, 1966, for reviews), provide strong for having thoughtfully read and commented on the manuscript. We also thank evidence for apportioning the NA into 4 subdivisions basedon Carrie Norita, Daniel Aklufi, and Carlos Arias (technical), Kris Trulock (photo- graphic), and Belle Wamsley (secretarial) for excellent assistance. cell size, packing density, and peripheral targets. Three of these Correspondence should be addressed to P. E. Sawchenko, The Salk Institute, subdivisions, or formations as they have beentermed, comprise P.O. Box 85800, San Diego, CA 92138. = Present address: The Johns Hopkins University, School of Medicine, Balti- the NA of the more classicaldescriptions, known for sometime more, MD 2 1205. to innervate branchiomeric derivatives in the head and neck. Copyright 0 1989 Society for Neuroscience 0270-6474/89/05 166% 15$02.00/O From rostra1 to caudal these subdivisions are the esophageal, The Journal of Neuroscience, May 1989, 9(5) 1669 or compact, formation (cf); the palatopharyngeal, or semicom- fibers, and terminals were mapped in the medulla using camera lucida pact, formation (scf); and the laryngeal, or loose, formation (If). techniques. Most animals that received PHA-L deposits also received 1 ~1 injec- The fourth subdivision, composedof scatteredcells lying ventral tions of a 5.0% aqueous suspension of True blue (Dr. Illing GmbH & to the branchiomeric subdivisions, was termed the external for- Co. KG) into the sheath surrounding the vagus nerve. These deposits mation (ef) and has been shown to innervate the heart (see were made at, or slightly rostra1 to, the level of the nodose ganglion and Bieger and Hopkins, 1987; Hopkins, 1987). retrogradely labeled cells in all subdivisions of the ambigual complex. Projections from the NTS to the NA have been suggestedby Zmmunohistochemistry. The available literature and our own material were screened in an effort to identify transmitter candidates in terminals numerous investigators. Retrograde transport studies have de- in the rostra1 NA or in cell bodies in the central part of the NTS. scribed all aspectsof the caudal NTS as projecting to the ven- Prosomatostatin-derived peptides appeared to meet these criteria, and trolateral medulla (Bieger, 1984; Stuesseand Fish, 1984; Ross antisera directed against 3 of these, somatostatin- 14 (SS-14) somato- etal., 1985; Lovick, 1986; Blessingetal., 1987; Dampney, 1987), statin- (SS-28). and somatostatin-28 ,-, , (SS-28 ,_,,). were used to iden- and anterogradetracing studiesemploying the autoradiographic tify the d~ominant molecular form(s). ‘Thk sera ‘e’mployed were those designated S3 10, S309, and S320, respectively, of Benoit et al. (1982a, method have described relatively diffuse projections from the b), and the results of cross-adsorption studies attesting to the specificity medial part of the NTS to this region (Loewy and Burton, 1978; of these sera were compatible with those provided by this (Sawchenko Norgren, 1978; Ricardo and Koh, 1978; Becksteadet al., 1980; et al., 1988) and other (Morrison et al., 1982, 1983) laboratories. Spe- Sawchenkoand Swanson, 1982; Rosset al., 1985). Interestingly, cifically, medullary staining with each antiserum was abolished follow- ing preadsorption with 30 mM concentrations of the respective synthetic only those casesin which tracer depositsinvolved the region of immunogens and was at most modestly attenuated by equimolar con- the rostra1 aspect of the NA displayed labeling of a relatively centrations of the other 2 heterologous prosomatostatin-derived pep- circumscribed cluster of neurons in the medial part of the NTS tides. (Bieger, 1984; Stuesseand Fish, 1984; Ross et al., 1985) a cell Three routes of colchicine administration were used so as to give maximal enhancement ofperikaryal staining in the NTS. These included group termed the central part of the NTS by Rossand colleagues direct injection of a solution containing 50 pg colchicine in 25 bl saline (1985). This region has been implicated both anatomically into a lateral ventricle, a similar injection into the cisternum magnum, (Fryscak et al., 1984; Altschuler et al., 1988) and physiologically or direct application of a pledget of Gelfoam soaked in the same solution (Jean, 1972a, b, 1978; Amri et al., 1984; Bieger, 1984) as re- to the dorsal surface of the medulla. Each procedure was performed 48-
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