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Enkephalin-Like Immunoreactivity of Olivocochlear Nerve Fibers In Proc. NatL Acad. Sci. USA Vol. 78, No. 2, pp. 1255-1259, February 1981 Neurobiology Enkephalin-like immunoreactivity of olivocochlear nerve fibers in cochlea ofguinea pig and cat (opioid/cholinergic neurons/organ ofCorti/immunofluorescence/efferent synapses) JORGEN FEX AND RICHARD A. ALTSCHULER Laboratory ofNeuro-otolaryngology, National Institute ofNeurological and Communicative Disorders and Stroke, National Institutes ofHealth, Bethesda, Maryland 20205 Communicated by William D. Neff, October 17, 1980 ABSTRACT The distribution ofenkephalin-like immunoreac- ents may cross at the tunnel floor (17). Large synaptic terminals tivity in the cochlea ofthe guinea pig and cat was studied. Indirect on outer hair cells are endings ofupper tunnel crossing fibers (9, immunofluorescence immunohistochemistry using antisera gen- 12, 16) and are efferent (18, 19). Smaller efferent endings form erated against a methionine enkephalin-bovine thyroglobulin con- jugate was applied to surface preparations of the organ of Corti synapses with auditory nerve dendrites at the outer hair cell and cryostat sections of the whole of the cochlea. In the cochlear bases (20, 21). The efferent innervation is maximal in the first osseous spiral lamina, immunofluorescence was localized to un- and second turns ofthe cochleaand diminishes towards the apex myelinated fibers ofthe intraganglionic spiral bundle. In the organ (22, 23). The large efferent endings on outer hair cells are totally of Corti, immunofluorescence was localized to a small number of (22) or subtotally (23) absent in the most apical part ofthe organ fibers at inner hair cells, the inner spiral bundle, and tunnel spiral ofCorti. bundle, to tunnel crossing fibers at the level ofthe tunnel floor, to an occasional spiral outer fiber, and to the synaptic region ofouter The efferent innervation of the organ of Corti was divided hair cells in the three rows of the basal turn of the cochlea. Less into crossed and uncrossed olivocochlear fibers, corresponding immunofluorescence was found in this region as one progressed to cells of origin that project to the contralateral or ipsilateral towards the apex, with none seen at the apex. At the most apical cochlea (24-26). Recently a case has been made for a different region the inner spiral bundle became patchy and the tunnel spiral dichotomy ofthe olivocochlear neurons (27-29). One system of bundle developed arcades. There was no immunofluorescence olivocochlear neurons is characterized by relatively small cell found in spiral ganglion cells, in auditory nerve fibers, or in the hair cells ofthe organ ofCorti. The findings were the same in cat bodies, located mostly in the lateral superior olivary region. as in guinea pig, the latter being studied in more detail. It was con- These cells give rise to both crossed and uncrossed thin, perhaps cluded that efferent, olivocochlear neurons ofthe cochlea, synaps- unmyelinated, axons that synapse with cells and auditory nerve ing predominantly with primary auditory nerve fibers from the in- dendrites predominantly in the region of inner hair cells (29). ner sensory cells or with the sensory cells, contain enkephalin-like The other system has larger cell bodies located mostly in the immunoreactivity. Also, the findings indicate that endings of oli- medial superior olivary region and trapezoid body. These cells vocochlear neurons that synapse predominantly with outer hair cells contain enkephalin-like immunoreactivity. It has previously send both crossed and uncrossed, perhaps myelinated, axons been shown that ofivocochlear neurons are likely to be cholinergic. that synapse predominantly with large endings on outer hair cells (29). Methionine enkephalin and leucine enkephalin are opioid pen- The functions of the cochlear efferents are unknown. There tapeptides originally isolated from the whole brain (1, 2). Im- is strong evidence that there are inhibitory olivocochlear neu- munohistochemical mapping of enkephalin-like immunoreac- rons (30, 31), cholinergic olivocochlear neurons (32-35), and tivity in the central nervous system was done (3-5), and it was olivocochlear neurons that form part of an auditory feedback noted that in certain regions enkephalin-like immunoreactivity loop (36, 37). It is not known ifthese categories completely over- and opiate receptors had a similar distribution (3, 5). A much lap or ifthere is a correspondence to the two systems ofmyelin- entertained working hypothesis is that enkephalins may act as ated and unmyelinated olivocochlear neurons. It is likely, how- neurotransmitters or modulate the action of neurotransmit- ever, that neurons ofboth systems contain acetylcholinesterase ters (6). (23, 38, 39). In the organ ofCorti, each inner hair cell synapses with about In the present study, using immunohistochemical tech- 20 auditory nerve boutons from about 90% of the total spiral niques, we have found enkephalin-like immunoreactivity in oh- ganglion cell population (7-9). The outer hair cells make rela- vocochlear efferent nerve fibers and in synaptic regions in the tively few synapses with auditory nerve boutons from about 10% organ ofCorti and in unmyelinated nerve fibers ofthe intragan- of the spiral ganglion cells (7-9). The auditory receptor organ glionic spiral bundle ofthe cochlea. also receives efferent, centrifugal innervation from the brain- stem, through olivocochlear neurons. In the cochlea, myelin- MATERIALS AND METHODS ated and unmyelinated olivocochlear fibers spiral in the fascicles ofthe intraganglionic bundle (10, 11) and then fan out to the or- Antiserum. Antibodies to methionine enkephalin were gen- gan of Corti. In the organ of Corti, such fibers form the inner erated in female New Zealand White rabbits by using methio- spiral bundle and the tunnel spiral bundle (12-14). Inner hair nine enkephalin (Boehringer Mannheim) coupled with glutar- cells and auditory nerve dendrites under inner hair cells receive aldehyde (Polysciences 70%, EM grade) to bovine thyroglobulin efferent innervation from the inner spiral bundle (15). The up- (Sigma type I), following procedures described in detail else- per tunnel crossing fibers are efferent (9, 16), and other effer- where (40, 41). Tissue Preparation. NIH strain guinea pigs ofboth sexes, 14 The publication costs ofthis article were defrayed in part by page charge young (85-145 g) and 28 mature (275-325 g), were used, mature payment. This article must therefore be hereby marked "advertise- animals for surface preparations and young animals for surface inent" in accordance with 18 U. S. C. §1734 solely to indicate this fact. preparations and cryostat sections. Cats were also examined, 3 1255 Downloaded by guest on September 26, 2021 1256 Neurobiology: Fex and Altschuler Proc. Natl. Acad. Sci. USA 78 (1981) mature (2-2.4 kg) and 1 young (0.9 kg). Guinea pigs were anes- nine or leucine enkephalin, the latter of much less intensity. thetized with chloral hydrate and perfused through the heart Antiserum to methionine enkaphalin was therefore used in sub- with 0.1 M sodium cacodylate buffer, pH 7.2, at 40C followed sequent experiments and the term "enkephalin" is used in de- by 4% (wt/vol) paraformaldehyde in 0.1 M sodium cacodylate scribing immunoreactivity. Structures were considered to ex- buffer at 40C. The temporal bones were removed, the cochleae hibit enkephalin-like immunoreactivity if they showed were exposed, and the inner ears were perfused with fixative immunofluorescent staining with enkephalin antisera and no through the round window. The cochleae were then rinsed. staining when the antiserum was absorbed with enkephalin Phosphate-buffered saline, pH 7.2, was used for all rinses. The (Fig. 1J). The fluorescence that was seen after such absorption bony shell and vascular stria ofeach cochlea were removed un- was considered nonspecific. Nonspecific fluorescence varied in der phosphate-buffered saline and the remaining cochlear spiral distribution and intensity between preparations and structures. with the organ of Corti was used for surface preparations or The tectorial membrane showed strong nonspecific fluores- cryostat sections. Cats were handled similarly to guinea pigs but cence. The basilar membrane often showed nonspecific fluores- were anesthetized with Nembutal. cence of variable intensity. The use of preimmune serum and Immunohistochemical Staining. Modifications of the indi- antisera against f3-endorphin and 13-lipotropin gave no specific rect immunofluorescence technique ofCoons (42) were used on immunofluorescence. The antiserum supplied by R. Elde gave both preparations. For surface preparations the cochlear spiral the same results as the antibody we generated, as did antiserum was incubated in a Beem capsule with 250 .1A of antiserum absorbed with thyroglobulin. against methionine enkephalin diluted 1:20. Phosphate-buff- A substance having immunoreactive sites identical to enke- ered saline with 0.3% Triton X-100 was used for all dilutions. phalin's could give the same immunocytochemical visualization The incubation proceeded for 25 min at 370C. A 1:200 dilution (43). For this reason the term "enkephalin-like immunoreactiv- with a 16-hr incubation at 40C was used interchangeably. After ity" was used. rinse, the second incubation was carried out with 250 A.l offlu- Methodological Considerations. In this study, the surface orescein isothiocyanate-labeled swine antiserum to rabbit im- preparations ofthe organ ofCorti gave excellent information on munoglobulin (Bio-Rad) diluted 1:10, for 25 min at 370C, fol-
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