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Ascending Projections from the Area Postrema and The Okajimas Folia Anat. Jpn., 75(1): 9-32, May, 1998 Ascending Projections from the Area Postrema and the Nucleus of the Solitary Tract of Suncus Murinus: Anterograde Tracing Study Using Phaseolus Vulgaris Leucoagglutinin By Hisao ITO and Makoto SEKI First Department of Anatomy, Hyogo College of Medicine, Mukogawa-cho 1-1, Nishinomiya, Hyogo 663-8501, Japan -Received for Publication, March 13, 1998- Key Words: Area postrema, Solitary nucleus, Suncus murinus, Vomiting, Phaseolus vulgaris leucoagglutinin Summary: Suncus murinus (suncus) is a new experimental animal model for research on the mechanisms underlying emesis. In the present study, we examined the ascending projections from the area postrema (AP) and the nucleus of the solitary tract (NTS) in suncus based on anterograde transport of phaseolus vulgaris leucoagglutinin. The AP pro- jected heavily to the dorsal vagal complex, especially in the commissural and medial subnuclei of the NTS, and the dorsal motor nucleus of the vagus. Some ascending fibers from the AP projected bilaterally to the parabrachial nucleus (Pb), but no labeling was observed rostral to this area. In contrast, the NTS had extensive projections as far as the basal forebrain. The NTS projections were observed in the AP, ventrolateral reticular formation including the nucleus ambiguus, A5 noradrenergic area, locus coeruleus, Pb, and central gray matter of the midbrain. At the level of the diencephalon, the NTS projections were seen in the dorsomedial, lateral, paraventricular, periventricular, supraoptic, retrochiasmatic and arcuate nuclei of the hypothalamus, in addition to the paraventricular nucleus of the thalamus. Terminal fields within the basal forebrain were also shown to include the medial preoptic area, the bed nucleus of the stria terminalis, the substantia innominata and the ventral pallidum. The results indicated that the neurological relationship between the chemo- and/or barosensitive systems including the trigger of the emetic response and the general viscerosensory and/or -motor systems may exist also in the suncus. Suncus murinus (suncus), a species of Insec- lie the emetic reflex via the AP. Some studies have tivora, is being used as a relatively new animal reported on the nature of the connectivity of the model for experimental research in Japan. Suncus AP, but most have used the rat as their model, are easily induced to vomit by exposing them to which, unlike the suncus, is not prone to vomit- various stimuli, e.g., the emetic agents nicotine and ing (van der Kooy and Koda, 1983; Shapiro and veratrine (Ueno et al., 1987), or reciprocal shaking Miselis, 1985a; Herbert et aL, 1990; Cunningham et (Ueno et aL, 1988), and this makes the suncus a aL, 1994). In the ferret, a species with a high inci- valuable experimental model for emetic research. dence of vomiting, Strominger et aL (1994) demon- The area postrema (AP) in the suncus, as in the strated that the AP has reciprocal connections only rat and rabbit, is an unpaired midline structure that with the nucleus of the solitary tract (NTS), which ocupies the wall of the obex of the fourth ventricle. is generally accepted as the primary recipient of It is a highly vascular structure with a very weak gustatory, cardiovascular, pulmonary, and gastro- blood-brain diffusion barrier, allowing most sub- intestinal sensory afferents. stances to penetrate into the interstitial space be- Studies on the innervation of the NTS have tween the neurons. Based on physiological studies, suggested that functionally classified columns are the AP has generally been recognized to act as a arrayed rostrocaudally in this nucleus; for example, "chemoreceptor trigger zone" for the induction of gustatory afferents occupy the rostral third portion emesis (Borison et al., 1984; Carpenter, 1989), how- of the column (Whitehead and Frank, 1983; Hamil- ever, there have been few morphological studies ton and Norgren, 1984), while visceral afferents concerning the neuronal mechanisms which under- occupy a more caudal region (Kalia and Mesulam , Correspondence to Dr. Hisao Ito, First Department of Anatomy, Hyogo College of Medicine , Mukogawa-cho 1-1, Nishinomiya, Hyogo 663-8501, Japan 9 10 H. Ito and M. Seki 1980; Panneton and Loewy, 1980; Ciriello, 1983; ture, postfixed with 4% paraformaldehyde in the Rogers and Hermann, 1983; Seiders and Stuesse, phosphate buffer overnight, and then stored in 20% 1984; Gwyn et aL, 1985; Shapiro and Miselis, 1985b; sucrose solution for 2 days. Frozen frontal or Sweazey and Bradley, 1986; Housley et al., 1987; sagittal sections were cut serially at a thickness of Norgren and Smith, 1988; Altschuler et al. , 1989, 40 gm with a freezing microtome, and every third 1991). Based on neurological studies showing that section was collected and treated for immunohisto- the NTS controls the gastrointestinal tract via the chemical PHA-L reaction. The procedures for dorsal motor nucleus of the vagus (DMV) (Morest, PHA-L were carried out according to Gerfen and 1967; Cottle and Calaresu, 1975; Norgren, 1978; Sawchenko (1984). In brief, the sections were Beckstead et aL, 1980; Rogers et aL, 1980; Arends treated with 1% albumin solution for 1 hour, and et al. , 1988), and controls the pharynx, larynx, and then incubated in rabbit anti-PHA-L serum (dilu- esophagus via the nucleus ambiguus (Amb) tion 1 : 2000, EY Lab.) for 2-3 days. The primary (Morest, 1967; Cottle and Calaresu, 1975; Loewy antibodies were localized by incubation in biotiny- and Burton, 1978; Norgren, 1978; Ricardo and Koh, lated goat anti-rabbit IgG serum (1 : 5000, Vector) 1978; Beckstead et al., 1980; ter Horst et aL, 1984; overnight, and then in an ABC kit (Vector) over- Ross et al., 1985; Arends et aL, 1988; Cunningham night at 4 °C. Between each incubation, the sections and Sawchenko, 1989; Cunningham et al., 1991), were rinsed thoroughly with a Tris-buffer solution the NTS appears to play an important role as the containing Triton-X100 at pH 7.4. After incubation, afferent system of all visceromotor reflexes, includ- peroxidase was visualized by the cobalt-glucose oxi- ing the emetic response. Nevertheless, to define the dase method with diaminobenzidine (DAB) (Itoh neural pathways involved in the vomiting reflex, et aL, 1979). After mounting on gelatin-coated further comparative studies are necessary, espe- slides, the sections were dehydrated in alcohol, cially in species having vomiting peculiarities. cleared in xylene, coverslipped, and observed The purpose of the present study was to examine under a light microscope. In order to clarify the in detail the ascending pathways and projection normal cytoarchitecture, adjacent sections on one targets of the AP as well as those of the viscero- side were stained with thionin. sensory region of the NTS of the suncus by using In order to investigate the relationship between the anterograde tracing method with Phaseolus anterograde labelings in the specific catechol- vulgaris leucoagglutinin (PHA-L). aminergic and peptidergic neurons, adjacent sec- tions on the opposite side were immunostained by the peroxidase-antiperoxidase (PAP) method Materials and Methods (Sternberger, 1979) using mouse anti-tyrosine hydroxylase (TH) (Chemicon, dilution 1 : 1000), The experiments were carried out on 68 adult rabbit anti-phenylethanolamine-N-methyltrans- suncus of both sexes. The males weighed 50-90 g, ferase (PNMT) (Chemicon, dilution 1 : 1000), and the females weighed 35-55 g; 57 animals were rabbit anti-arginine vasopressin (AVP) (Chemicon, used for the PHA-L anterograde tracing study and dilution 1 : 2000) and rabbit anti-oxytocin (OT) 11 for the fluoro-gold (FG) retrograde tracing study. (Funakoshi, dilution 1 : 500) sera. Each section was All surgical procedures were carried out under so- incubated with the respective primary antiserum dium pentobarbital anesthesia (40-50 mg/kg, i.p.). for 2 days at 4 °C, and subsequently treated with a The cytoarchitectonic identifications and the brain secondary antibody (goat anti-mouse IgG; Cappel, nomenculture are according to the descriptions of dilution 1 : 100 or anti-rabbit IgG; Cappel, dilution Paxinos and Watson (1986) in the rat. 1 : 100) and a final third layer (mouse PAP; Dako, In the anterograde tracing experiments, injec- dilution 1 : 100 or rabbit PAP; Dako, dilution tions of 2.5% PHA-L (Hohnen Inc., in 0.1 M Tris- 1 : 400) overnight at 4 °C. The immunoreaction was buffer solution containing 0.3 M KC1 at pH 8.2) visualized by DAB reaction. were made into either the AP or the NTS. The To confirm the results of the anterograde tracing tracer was injected iontophoretically with a current study by retrograde transport, 0.02-0.04 gl of of 10-20 gA applied in an alternating mode (5 s 1% FG (Fluorochrome Inc.) was injected into the on/5 s off). Seven to ten days after the injection, the parabrachial nucleus (Pb) under pressure with a 1 animals were perfused with 50 ml saline, followed gl Hamilton syringe. Two days after the microinjec- by 100 ml of a solution containing 4% paraformal- tion, the animals were anesthetized and perfused dehyde and 0.1% glutaraldehyde in 0.1 M phos- transcardially with 50 ml saline, followed by 300 ml phate buffer at pH 7.2, and then with 250 ml of 4% of a solution containing 4% paraformaldehyde in paraformaldehyde. The brains were immediately phosphate buffer. The brains were removed and removed and embedded in an agarose-gelatin mix- embedded in an agarose-gelatin mixture, postfixed Area Postrema and Solitary Nucleus Projections in the Suncus 11 with the same fixative overnight, then stored in extent of the injection site in animal No. 47, in- 20% sucrose solution for 2 days. Serial frontal fro- cluding the entire DVC with slight overlap into zen sections were cut at a thickness of 40 pm with regions immediately lateral and ventral to it (i.e., a freezing microtome, mounted on slides, and air- the gracile and the hypoglossal (XII) nuclei, respec- dried at room temperature.
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