Afferent Projections of the Trigeminal Nerve in the Goldfish, Carassius Auratus R.L
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JOURNAL OF MORPHOLOGY 198:131-147 (1988) Afferent Projections of the Trigeminal Nerve in the Goldfish, Carassius auratus R.L. PUZDROWSKI Department ofBioZogy, The University of Michigan, Ann Arbor. Michigan 48109 ABSTRACT The horseradish peroxidase (HRP) histochemical technique was used to examine the peripheral distribution and afferent projections of the trigeminal nerve in the goldfish, Carassius auratus. Sensory fibers of the trigeminal nerve distribute over the head via four branches. The ophthalmic branch distributes fibers to the region above the eye and naris. The maxillary and mandibular branches innervate the regions of the upper and lower lip, respectively. A fourth branch of the trigeminal nerve was demonstrated to be present in the hyomandibular trunk. Upon entering the medulla the trigeminal afferent fibers divide into a rostro- medially directed bundle and a caudally directed bundle. The rostromedially directed bundle terminates in the sensory trigeminal nucleus (STN) located within the rostral medulla. The majority of fibers turn caudally, forming the descending trigeminal tract. Fibers of the descending trigeminal tract termi- nate within three medullary nuclei: the nucleus of the descending trigeminal tract (NDTV), the spinal trigeminal nucleus (Spv), and the medial funicular nucleus (MFn). All projections, except for those to the MFn, are ipsilateral. Contralateral projections were observed at the level of the MFn following the labeling of the ophthalmic and maxillomandibular branches. All branches of the trigeminal nerve project to all four of the trigeminal medullary nuclei. Projections to the STN and MFn were found to be topographically organized such that the afferents of the ophthalmic branch project onto the ventral portion of these nuclei, while the afferents of the maxillo- and hyomandibular branches project to the dorsal portion of these nuclei. Cells of the mesencephalic trigeminal nucleus were retrogradely labeled following HRP application to the ophthalmic, maxillary, and mandibular branches of the trigeminal nerve. In addition to demonstrating the ascending mesencephalic trigeminal root fibers, HRP application to the above-mentioned branches also revealed descending mesencephalic trigeminal fibers. The de- scending mesencephalic trigeminal fibers course caudally medial to the bran- chiomeric motor column and terminate in the ventromedial portion of the MFn. As in most anamniotic gnathostomes, the '67; Harrison, '81). trigeminal sensory nerve in teleosts consists In teleosts the afferent fibers of the trigem- of maxillomandibular branches, which dis- inal nerve enter the brainstem as a single tribute fibers to the oral region, and an root that distributes fibers to the trigeminal ophthalmic branch, which distributes fibers medullary nuclear complex (Woodburne, '36; to the region dorsal to the orbit and naris. In Luiten, '75). In addition to these sensory af- addition, in teleosts a third branch of the ferents, fibers from the cells of the mesence- trigeminal nerve, termed the ramus com- phalic trigeminal nucleus exit the brainstem municans, has been described coursing pe- through the trigeminal root and course pe- ripherally along the rostral operculum as a ripherally in the branches of the trigeminal part of the hyomandibular trunk (Herrick, nerve. 1899; Allis, '03; Maheshwari, '65; Saxena, There have been relatively few studies uti- G 1988 ALAN R. LISS, INC 132 R.L. PUZDROWSKI lizing modern tracing techniques to investi- trigeminal nucleus. A third specimen (ap- gate the primary afferents of the sensory trigeminal nerve in teleosts. Using degener- A hhreviatwns ation methods to investigate the projections of the entire trigeminal root in the carp (Cy AG anterior ganglion prinus carpw), Luiten ('75) reported that the ALLN root of the anterior lateral line nerve descending trigeminal tract gives off axons ALLNd dorsal root of the anterior lateral line nerve ALLN, ventral root of the anterior lateral line to four different cell groups, which he consid- nerve ered subdivisions of the nucleus of the de- BS bulbospinal tract scending trigeminal tract. There has been Cb cerebellum only a single study of the trigeminal sensory cc cerebellar crest afferents utilizing horseradish peroxidase CL caudal lobe of the cerebellum DTN dorsal tegmental nucleus (HRP) techniques in two species of teleosts, DTV descending trigeminal tract Hypsoblennius and Oxylebius (von Bartheld EG eminentia granularis and Meyer, '85). That study was limited to FL facial lobe Fm facial motor nerve an examination of the afferent projections of FR fasciculus retroflexus the trigeminal nerve branches innervating Fs facial sensory nerve the cirri (finger-like projections found on the HYO hyomandibular trunk dorsal surface of the head in these genera) I11 third ventricle IL inferior lobe of the hypothalamus and its findings agreed, for the most part, I0 infraorbital trunk with the description given by Luiten ('75). IR inferior reticular formation The mesencephalic trigeminal nucleus has Iv fourth ventricle been described in a number of teleosts (Wein- LLF lateral longitudinal fasciculus MA Mauthner axon berg, '28; Woodburne, '36; Luiten, '75, '79). MAN mandibular branch of the infraorbital trunk However, the peripheral distribution of the MAX maxillary branch of the infraorbital trunk afferents of these cells has never been fullv MFn medial funicular nucleus examined, nor has a mesencephalic trigemi- medial longitudinal fasciculus MR medial reticular formation nal root ever been experimentally demon- Mv cells of the mesencephalic trigeminal strated in a teleost. nucleus The purpose of the present study was to nC commissural nucleus of Cajal provide a complete description of the primary Nm nucleus of the descending trigeminal tract NMLF nucleus of the medial longitudinal sensory afferents of the trigeminal nerve in fasciculus a teleost, the goldfish Carassius auratus, uti- oPv ventricle of the optic tectum lizing HRP techniques. An abstract of this OT optic tectum work has been published previously Cpuz- pal palatine ramus of the facial sensory nerve PC posterior commissure drowski, '85). PCT posterior cerebellar tract PG preglomerular complex MATERIALS AND METHODS PN periventricular nucleus of the inferior lobe The results of this study are based on ob- rcl Communicating ramus of the trigeminal nerve servations made using 32 goldfish, C. aura- rosl lateral line ramus of the supraorbital trunk tus, ranging in size from 1-12 cm in total ros, trigeminofacial ramus of the supraorbital length. All surgical and perfusion procedures v+vii trunk otic ramus of the lateral line nerve utilized animals that were anesthetized with Et recurrent ramus of the facial sensory nerve tricaine methane sulfonate (Sigma Chemical ~IIroot of the facial sensory nerve Co., St. Louis, MO). SG secondary gustatory tract Five animals were used for survey pur- SGN secondary gustatory nucleus supraorbital trunk poses. Two specimens were transcardially so spinal trigeminal nucleus perfused with 0.04 M phosphate buffer and superior reticular formation MA(90 ml80% ethanol, 5 ml stock formal- STN sensory trigeminal nucleus dehyde, 5 ml glacial ascetic acid); the brains T dorsal thalamus torus longitudinalis were removed, embedded in Paraplast &an- :L root of the trigeminal nerve cer, Distributors, St. Louis, MO), and serially Val" valvula of the cerebellum sectioned in the transverse plane at 10 pm. VII root of the facial sensory nerve These sectioned brains were subsequently VIIm facial motor nucleus vagal lobe stained with cresyl violet and used to exam- ;k trigeminal motor nucleus ine the normal anatomy of the brainstem Xm vagal motor nucleus trigeminal centers and the mesencephalic XN vagus nerve Fig. 1. Lateral view of the head of Carassius auratus HRP application. The outline of the brain is indicated illustrating the distribution of the supraorhital, infraor- by dots; the outline of the body is indicated by dashes. hital, and hyomandihular nerve trunks over the head. Bar scale = 1 mm. Arrowheads indicate points of nerve transection and proximately 1 cm in length) was prepared Hawk International, Distributors, Montreal, according to the Bodian reduced silver pro- Canada). The location of HRP application to cedure and used to examine the peripheral each trunk is illustrated in Figure 1. When distribution of the main nerve trunks carry- labeling the nerves that course along the ing trigeminal rami. The peripheral distri- walls of the orbit (SO, 10, MAX, and MAN, bution of the nerve trunks of the head was see Fig. 1) the eyeball was retracted, the also examined in two specimens that had nerve transected and labeled with HRP, and been prepared by a modification of the Sihler the eyeball then replaced and covered with technique (Freihofer, '66). Specimens pro- histoacryl. The hyomandibular trunk was cessed by this technique are rendered trans- transected and labeled with HRP at the point parent, except for the nerves, which are in the rostrodorsal wall of the opercular cav- stained a dark purple. ity where it courses superficially before en- Surgical procedures were performed with tering the hyomandibular bone. The palatine the aid of a Zeiss stereozoom operating mi- ramus was labeled with HRP at a point croscope. Following anesthetization, the fish where it courses along the posterior wall of was wrapped in moistened cheesecloth and the orbit in order to establish that it was a individual nerve trunks were exposed and branch of the facial sensory nerve containing