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Trigeminal Ganglion Innervates the Auditory Brainstem

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Trigeminal Ganglion Innervates the Auditory Brainstem THE JOURNAL OF COMPARATIVE NEUROLOGY 419:271–285 (2000) Trigeminal Ganglion Innervates the Auditory Brainstem SUSAN E. SHORE,1,2* ZOLTAN VASS,3 NOEL L. WYS,1 AND RICHARD A. ALTSCHULER1 1Kresge Hearing Research Institute, University of Michigan, Ann Arbor, Michigan 48109-0506 2Department of Otolaryngology, Medical College of Ohio, Toledo, Ohio 43699 3Department of Otolaryngology, Albert Szent-Gyorgyi Medical University, Szeged, Hungary ABSTRACT A neural connection between the trigeminal ganglion and the auditory brainstem was investigated by using retrograde and anterograde tract tracing methods: iontophoretic injec- tions of biocytin or biotinylated dextran-amine (BDA) were made into the guinea pig trigem- inal ganglion, and anterograde labeling was examined in the cochlear nucleus and superior olivary complex. Terminal labeling after biocytin and BDA injections into the ganglion was found to be most dense in the marginal cell area and secondarily in the magnocellular area of the ventral cochlear nucleus (VCN). Anterograde and retrograde labeling was also seen in the shell regions of the lateral superior olivary complex and in periolivary regions. The labeling was seen in the neuropil, on neuronal somata, and in regions surrounding blood vessels. Retrograde labeling was investigated using either wheatgerm agglutinin- horseradish peroxidase (WGA-HRP), BDA, or a fluorescent tracer, iontophoretically injected into the VCN. Cells filled by retrograde labeling were found in the ophthalmic and mandib- ular divisions of the trigeminal ganglion. We have previously shown that these divisions project to the cochlea and middle ear, respectively. This study provides the first evidence that the trigeminal ganglion innervates the cochlear nucleus and superior olivary complex. This projection from a predominantly somatosensory ganglion may be related to integration mechanisms involving the auditory end organ and its central targets. J. Comp. Neurol. 419: 271–285, 2000. © 2000 Wiley-Liss, Inc. Indexing terms: pathways; cochlear nucleus; lateral superior olivary complex; olivocochlear; somatosensory It is well established that somatosensory stimuli evoke directly to the dorsal cochlear nucleus (DCN) and the responses in auditory neurons (Aitkin et al., 1978, 1981). granule cell region of the ventral cochlear nucleus (Itoh et Such multisensory integration may play a role in localiz- al., 1987; Weinberg and Rustioni, 1987). A projection from ing the body in space, once attributed only to higher cen- the cuneate nucleus gives rise to mossy fiber terminals in ters such as the superior colliculus where auditory, so- the dorsal DCN and granule cell domains of the cochlear matosensory, and visual inputs converge (Drager and nucleus (Wright and Ryugo, 1996). These projections may Hubel, 1976; Chalupa and Rhoades, 1977). The trigeminal be excitatory or inhibitory (Saade et al., 1989; Young et al., system is one major component of this integration, con- 1995) as demonstrated by electrical stimulation and tac- tributing a major source of somatosensory input to the superior colliculus from the brainstem trigeminal complex (Killackney and Erzurumlu, 1981). More recent neuroana- Grant sponsor: NIH; Grant numbers: 5RO1DC00383, RO1 DC 000105; tomical data indicate that somatosensory and auditory Grant sponsor: National Organization of Hearing Research (NOHR); Grant information converge at more peripheral sites. First-order sponsor: Fogerty International; Grant number: TW 00502. relay somatosensory neurons, which subserve tactile and *Correspondence to: S.E. Shore, Ph.D., Kresge Hearing Research Insti- tute, University of Michigan, 1301 E. Ann St., Ann Arbor, MI 48109. kinesthetic sensations, send direct projections to the co- E-mail: [email protected] chlear nucleus: for example, the dorsal column nuclei and Received 2 August 1999; Revised 2 November 1999; Accepted 2 Decem- interpolar and caudal spinal trigeminal nuclei send fibers ber 1999 © 2000 WILEY-LISS, INC. 272 S.E. SHORE ET AL. tile manipulation of the pinna (Young et al., 1995). Be- Anterograde tracing cause changes in pinna position provide important spec- Injections using biocytin and BDA. tral cues for sound localization (Rice et al., 1992), Biocytin and bi- somatosensory input to the cochlear nucleus regarding otinylated dextran-amine (BDA) injections were made pinna position may aid in sound localization performed by into the trigeminal ganglion, and anterograde labeling DCN cells. Somatosensory innervation of the cochlear nu- was examined in the cochlear nucleus, a light microscopic cleus or superior olivary complex may also be involved in evaluation in five animals and an electron microscopic mechanisms related to neck movements, which play a role evaluation in two animals. The location of the trigeminal in orientation to acoustic stimuli. ganglion was identified by using stereotaxic coordinates The present investigation demonstrates that second- (0.37 cm caudal to bregma, 0.45 cm lateral from midline, order auditory neurons in the cochlear nucleus are inner- 1.3 cm ventral to bregma), a small hole was drilled in the vated by both the ophthalmic and mandibular divisions of skull without disturbing the meninges, and a glass mi- ␮ the trigeminal ganglion, which also project to the cochlea cropipette (tip diameter 25–30 m) was lowered 13 mm by and middle ear, respectively (Vass et al., 1997, 1998b). micromanipulator into the left trigeminal ganglion. Ionto- The ophthalmic division of the trigeminal ganglion also phoretic injections of biocytin or BDA were delivered via a innervates the extraocular muscles (Aigner et al., 1997), glass microelectrode by using a constant current genera- ␮ raising the interesting possibility of interactions among tor (Stoelting, 3 A alternating for 20 minutes). Biocytin these three systems. A second major finding indicates that (Sigma Chemical Co., St. Louis, MO; B-4261) was pre- a reciprocal connection exists between neurons in the shell pared as a 5% solution in 0.05 M Tris buffer (pH 7.6). The regions of the lateral superior olivary complex and the solution could be stored at 4°C for up to 7 days with no trigeminal ganglion. Together with the trigeminal gan- noticeable loss of activity. Dental cement was used to seal glion innervation of the small cell cap region of the an- the opening, the overlying skin was sutured, and the an- teroventral cochlear nucleus (AVCN), this projection may imals were allowed to recover. form part of the olivocochlear feedback system. Light microscopic assessment. Twenty-four hours after the biocytin and 4–6 days after BDA injections, animals were euthanized. Each guinea pig was anesthe- MATERIALS AND METHODS tized with nembutal (15 mg/kg, i.p.) and ketamine (40 All experiments were carried out in accordance with the mg/kg, i.m.) and perfused through the left ventricle of the NIH Guide For the Care and Use of Laboratory Animals. heart with 200 ml of 0.1 M pH 7.4 phosphate buffer, Twelve pigmented guinea pigs (250–350 g; NIH Outbred followed by 200 ml of 1% paraformaldehyde and 1.5% strain, Murphy Breeding Laboratory, Plainfield, IN) were glutaraldehyde in 0.1 M phosphate buffer, pH 7.2–7.4. The used in this study. The guinea pigs were anesthetized flow of the fixative to the trigeminal ganglia and brain- with ketamine hydrochloride (Ketaset; 80 mg/kg) and xy- stem by way of the common carotid arteries was maxi- lazine (Rompun; 4 mg/kg) and placed in a stereotaxic mized by occluding the brachial arteries and the descend- frame (David Kopf, Tujunga, CA), then a longitudinal ing aorta. Following perfusion-fixation, both the brain and incision was made in the scalp. Periodic drug supplements trigeminal ganglia were isolated and placed in fresh fixa- were used to maintain anesthetic levels throughout the tive (2% paraformaldehyde and 2.5% glutaraldehyde in procedure. 0.1 M phosphate buffer, pH 7.2–7.4) for 2–4 hours at 4°C. The tissues were then incubated overnight at 4°C with 30% sucrose in 0.1 M phosphate buffer. Each specimen was frozen with dry ice in 100% ethanol and frozen transverse sections obtained serially at 30-␮m Abbreviations increments on a sliding microtome. For BDA and biocytin, AVCN anteroventral cochlear nucleus the sections were first incubated for 2 hours in Avidin-D- AVII accessory facial nucleus horseradish peroxidase (HRP; Vector Laboratories, Inc., BDA biotinylated dextran amine Burlingame, CA; #A-2004), in 0.1 M phosphate buffer with DAB 3,3Ј-diaminobenzidine tetrahydrochloride 1% Triton X-100 (Sigma 9002-93-1), pH 7.4, and then DCN dorsal cochlear nucleus 1 LNTB lateral nucleus of the trapezoid body reacted with 3,3 -diaminobenzidine tetrahydrochloride LPO lateral periolivary region (DAB). Slides were counterstained for 3.5 minutes in 1% LSO lateral superior olivary complex aqueous neutral red (J.T. Baker Inc., Phillipsburg, NJ, R Mand mandibular division 747-03; Mesulam, 1978), buffered at pH 4.8 with acetate Max maxillary division MSO medial superior olivary complex buffer. The slides were washed in distilled H2O, dehy- MTB medial nucleus of the trapezoid body drated in graded EtOH, cleared in xylene, coverslipped by M5 motor nucleus of the fifth cranial (trigeminal) nerve using Permount, and studied using a Leitz Dialux micro- OCA octopus cell area scope equipped with a drawing tube. Oph ophthalmic division PN pontine nucleus Slides were examined by using brightfield microscopy to PR5 principal trigeminal nucleus locate and map labeled neurons located in the trigeminal PVCN posteroventral cochlear nucleus ganglion injection site and anterograde labeling of neuron RN raphe nucleus puncta in the auditory brainstem. Photomicrographs and RPO rostral periolivary region R7 root of the 7th cranial nerve camera lucida drawings were digitized and imported to SCC small cell cap of the VCN Adobe Photoshop for labeling and contrast adjustment. ST5 spinal trigeminal nucleus Electron microscopic evaluation. Three guinea pigs TZ trapezoid body were processed for electron microscopy, two 24 hours after VCN ventral cochlear nucleus VNTB ventral nucleus of the trapezoid body biocytin and one 4–6 days after BDA injections were made WGA-HRP wheatgerm agglutinin-horseradish peroxidase into ventral cochlear nucleus (VCN) as described above.
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