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01-12-2003 | Research Article

Diversity of axonal ramifications belonging to single lateral and medial olivocochlear neurons

Authors: W. Bruce Warr, Jo Ellen Boche

Published in: Experimental Brain Research | Issue 4/2003

Abstract

A classification of olivocochlear (OC) neurons based on their location in either the lateral or medial region of the superior olivary complex provides a powerful tool for predicting their terminations beneath the inner (IHC) or outer hair cells (OHC) of the cochlea, respectively. Yet the morphology of axonal terminations belonging to single lateral OC (LOC) and medial OC (MOC) neurons, which can provide clues about the functional capabilities of individual efferent neurons, has been relatively unexplored. Following injections of biotinylated dextran amine into regions containing OC neurons in the rat, we reconstructed 19 LOC and 15 MOC axons in surface preparations of the cochlea. Confirming previous studies, LOC axons could be classified as either intrinsic or shell based on the length (short versus long) of their terminal ramifications beneath the IHC. However, intrinsic LOC axons were of two types, those that traveled to the organ of Corti without branching (simple intrinsic) and those that had three or more branches that converged on the same discrete patch of IHCs (converging intrinsic). Regarding shell neurons, we found that they may have as many as four intraganglionic branches that could innervate as much as 41% of cochlear length. Lastly, we found that MOC neurons were extremely diverse, not only in the number of their tunnel-crossing fibers (1–15), but also in both the number of boutons they formed (1–48) and in their basal–apical spans (1–45%). Analysis revealed that the number of tunnel-crossing fibers formed by a given axon was closely related to the total number of its terminal boutons, but not to its cochlear span. Analysis further suggested the existence of two distinct subtypes of MOC neurons on the basis of the number of tunnel-crossing fibers and boutons each possessed: the more common sparsely-branched and the quite rare highly-branched MOC neurons. In conclusion, the variety of axonal ramifications of individual LOC and MOC neurons has functional implications and raises the question of whether the various types of efferent neurons might be subject to selective control by ascending and descending central auditory and possibly non-auditory pathways.

Adams JC (1981) Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775PubMed

Altschuler RA, Fex J, Parakkal MH, Eckenstein F (1984) Colocalization of enkephalin-like and choline acetyltransferase-like immunoreactivities in olivocochlear neurons of the guinea pig. J Histochem Cytochem 32:839–843PubMed

Aschoff A, Ostwald J (1988) Distribution of cochlear efferents and olivo-collicular neurons in the brainstem of rat and guinea pig: a double labeling study with fluorescent tracers. Exp Brain Res 71:241–251PubMed

Brandt HM, Apkarian AV (1992) Biotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey. J Neurosci Methods 45:35–40PubMed

Brown MC (1987) Morphology of labeled efferent fibers in the guinea pig cochlea. J Comp Neurol 260:605–618PubMed

Brown MC (1989) Morphology and response properties of single olivocochlear fibers in the guinea pig. Hear Res 40:93–109CrossRefPubMed

Burda H, Ballast L, Bruns V (1988) Cochlea in old world mice and rats (Muridae). J Morphol 198:169–285

Dannhof BJ, Bruns V (1993) The innervation of the organ of Corti in the rat. Hear Res 66:8–22CrossRefPubMed

Engstrom H, Ades HW, Andersson A (1966) Structural pattern of the organ of Corti. Williams & Wilkins, Baltimore

Greenwood DD (1961) Critical bandwidth and the frequency coordinates of the basilar membrane. J Acoust Soc Am 33:1344–1356

Guinan JJ, Warr WB, Norris BE (1983) Differential olivocochlear projections from lateral versus medial zones of the superior olivary complex. J Comp Neurol 221:358–373PubMed

Horvath M, Kraus KS, Illing RB (2000) Olivocochlear neurons sending axon collaterals into the ventral cochlear nucleus of the rat. J Comp Neurol 422:95–105CrossRefPubMed

Kakei S, Na J, Shinoda Y (2001) Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex. J Comp Neurol 437:170–185CrossRefPubMed

Le Prell CG, Bledsoe SC Jr, Bobbin RP, Puel JL (2001) Neurotransmission in the inner ear: functional and molecular analysis. In: Santos-Sacchi J, Jahn AF (eds) Physiology of the ear. Singular Publishing, New York, pp 575–611

Liberman MC (1980) Efferent synapses in the inner hair cell area of the cat cochlea: an electron microscopic study of serial sections. Hear Res 3:189–204

Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17–36CrossRefPubMed

Mathisen JS, Blackstad TW (1964) Cholinesterase in the hippocampal region. Distribution and relation to architectonics and afferent systems. Acta Anat (Basel) 56:216–253

Mulders WH, Robertson D (2000a) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hear Res 144:65–72CrossRefPubMed

Mulders WH, Robertson D (2000b) Morphological relationships of peptidergic and noradrenergic nerve terminals to olivocochlear neurones in the rat. Hear Res 144:53–64CrossRefPubMed

Müller M (1991) Frequency representation in the rat cochlea. Hear Res 51:247–254CrossRefPubMed

Osen KK, Mugnaini E, Dahl A-L, Christiansen AH (1984) Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cells system. Arch Ital Biol 122:169–212PubMed

Parent M, Levesque M, Parent A (2001) Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J Comp Neurol 439:162–175CrossRefPubMed

Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, Orlando

Puria S, Guinan JJ Jr., Liberman MC (1996) Olivocochlear reflex assays: effects of contralateral sound on compound action potentials versus ear-canal distortion products. J Acoust Soc Am 99:500–507PubMed

Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG (2000) Pathway tracing using biotinylated dextran amines. J Neurosci Methods 103:23–37CrossRefPubMed

Robertson D (1985) Brainstem location of efferent neurones projecting to the guinea pig cochlea. Hear Res 20:79–84CrossRefPubMed

Robertson D (1996) Physiology and morphology of cells in the ventral nucleus of the trapezoid body and rostral periolivary regions of the rat superior olivary complex studied in slices. Auditory Neurosci 2:15–31

Robertson D, Gummer M (1985) Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hear Res 20:63–77CrossRefPubMed

Robertson D, Winter IM (1988) Cochlear nucleus inputs to olivocochlear neurones revealed by combined anterograde and retrograde labelling in the guinea pig. Brain Res 462:47–55CrossRefPubMed

Safieddine S, Eybalin M (1992) Triple immunofluorescence evidence for the coexistence of acetylcholine, enkephalins, and calcitonin gene-related peptide within efferent olivocochlear neurons in rats and guinea-pigs. Eur J Neurosci 4:981–992PubMed

Safieddine S, Prior AM, Eybalin M (1997) Choline acetyltransferase, glutamate decarboxylase, tyrosine hydroxylase, calcitonin gene-related peptide and opioid peptides coexist in lateral efferent neurons of rat and guinea-pig. Eur J Neurosci 9:356–367PubMed

Santi P (1986) Organ of Corti surface preparations for computer assisted morphometry. Hear Res 24:179–187CrossRefPubMed

Satake M, Liberman MC (1996) Morphological subclasses of lateral olivocochlear terminals? Ultrastructural analysis of inner spiral bundle in cat and guinea pig. J Comp Neurol 371:621–632CrossRefPubMed

Thompson AM, Thompson GC (1991) Posteroventral cochlear nucleus projections to olivocochlear neurons. J Comp Neurol 303:267–285PubMed

Thompson AM, Thompson GC (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335:402–412PubMed

Thompson AM, Thompson GC (1995) Light microscopic evidence of serotoninergic projections to olivocochlear neurons in the bush baby (Otolemur garnettii). Brain Res 695:263–266CrossRefPubMed

Tokunaga A (1988) Superior olivary and lateral lemniscal neurons projecting to the cochlea in the guinea pig. Neurosci Res 6:20–30CrossRefPubMed

Veenman CL, Reiner A, Honig MG (1992) Biotinylated dextran amine as an anterograde tracer for single and double-labelling studies. J Neurosci Methods 41:239–254PubMed

Vetter DE, Mugnaini E (1992) Distribution and dendritic features of three groups of rat olivocochlear neurons. A study with two retrograde cholera toxin tracers. Anat Embryol (Berl) 185:1–16

Vetter DE, Adams JC, Mugnaini E (1991) Chemically distinct rat olivocochlear neurons. Synapse 7:21–43PubMed

Vetter DE, Saldana E, Mugnaini E (1993) Input from the inferior colliculus to medial olivocochlear neurons in the rat: a double label study with PHA-L and cholera toxin. Hear Res 70:173–186CrossRefPubMed

Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer-Verlag, New York Berlin Heidelberg, pp 410–448

Warr WB, Beck JE (1996) Multiple projections from the ventral nucleus of the trapezoid body in the rat. Hear Res 93:83–101CrossRefPubMed

Warr WB, Guinan JJJ, White JS (1986) Organization of the efferent fibers: the lateral and medial olivocochlear systems. In: Altschuler RA, Hoffman DW, Bobbin RP (ed) Neurobiology of hearing: the cochlea. Raven Press, New York, pp 333–348

Warr WB, Beck Boche J, Neely ST (1997) Efferent innervation of the inner hair cell region: origins and terminations of two lateral olivocochlear systems. Hear Res 108:89–111CrossRefPubMed

Warren EH III, Liberman MC (1989) Effects of contralateral sound of auditory-nerve responses. I. Contributions of cochlear efferents. Hear Res 37:89–104CrossRefPubMed

White JS, Warr WB (1983) The dual origins of the olivocochlear bundle in the albino rat. J Comp Neurol 219:203–214PubMed

Wilson JL, Henson MM, Henson OW (1991) Course and distribution of efferent fibers in the cochlea of the mouse. Hear Res 55:98–108CrossRefPubMed

Wouterlood FG, Jorritsma-Byham B (1993) The anterograde neuroanatomical tracer biotinylated dextran-amine: comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. J Neurosci Methods 48:75–87PubMed

Xiao Z, Suga N (2002) Modulation of cochlear hair cells by the auditory cortex in the mustached bat. Nat Neurosci 5:57–63CrossRefPubMed

Ye Y, Machado DG, Kim DO (2000) Projection of the marginal shell of the anteroventral cochlear nucleus to olivocochlear neurons in the cat. J Comp Neurol 420:127–138CrossRefPubMed

Title: Diversity of axonal ramifications belonging to single lateral and medial olivocochlear neurons
Authors: W. Bruce Warr
Jo Ellen Boche
Publication date: 01-12-2003
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 4/2003
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-003-1682-3

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Diversity of axonal ramifications belonging to single lateral and medial olivocochlear neurons

Abstract

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Abstract

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