Immunfluorescence study of neuropeptides in identified neurons of the rat auditory superior olivary complex (original) (raw)

Abstract

The present study was conducted to investigate the distribution and immunohistochemical characteristics of ascending and descending projection neurons of the rat superior olivary complex (SOC), a group of interrelated brainstem nuclei. Ascending neurons were identified by injection of cholera toxin B subunit (CTB) into the central nucleus of the inferior colliculus (IC), descending neurons were labeled by application of Fluoro-Gold (FG) into the scala tympani of the cochlea, ipsilaterally to the IC injection. In accordance with the literature, we observed neurons innervating the IC located in the lateral superior olivary nucleus (LSO) and dorsal periolivary groups (DPO) on both sides, in the superior paraolivary nucleus (SPO) predominantly ipsilateral, as well as in the ipsilateral medial superior olivary nucleus (MSO) and the medial nucleus of the trapezoid body (MNTB). Cochlear projection neurons were found predominantly in the ipsilateral LSO as well as in the bilateral SPO, DPO, MSO and MNTB. In addition, a considerable population of neurons in the ipsilateral LSO and SPO were identified as being both ascending and descending. To further characterize these double-projecting neurons, brainstem sections were incubated in antisera directed against different neuroactive substances. The majority of ascending/descending cells in the LSO contained calcitonin gene-related peptide, but not substance P (SP), met-enkephalin (ENK) or tyrosine hydroxylase (TH). Some of these neurons apparently were contacted by ENK-or SP-immunoreactive fibers and terminals. In addition, we found TH-immunoreactive neurons in the lateral MNTB region. These neurons, which were labeled upon tracer injection into the cochlea (but not upon IC injection), probably belong to the C1 catecholaminergic cell group and may represent a division of the uncrossed olivocochlear bundle. The present results reveal the existence of a previously unknown subpopulation of SOC neurons that project to both the cochlea and the inferior colliculus. Their CGRP immunoreactivity and their uncrossed projection pattern provide evidence that they may belong to the cholinergic, putatively excitatory cell group.

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (34)

  1. 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 71:241-251
  2. Eybalin M (1993) Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol Rev 73:309-373
  3. Eybalin M, Pujol R (1989) Cochlear neuroactive substances. Arch Otorhinolaryngol 246:228-234
  4. Fex J, Altschuler RA (1986) Neurotransmitter-related immunocy- tochemistry of the organ of Corti. Hearing Res 22:249-263
  5. Gil-Loyzaga PE (1995) Neurotransmitters of the olivocochlear lat- eral efferent system: with an emphasis on dopamine. Acta Otolaryngol 115:222-226
  6. Guinan JJ (1996) Physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RR (eds) The cochlea. Springer-Verlag, New York Berlin Heidelberg, pp 435-502
  7. Helfert RH, Bonneau JM, Wenthold RJ, Altschuler RA (1989) GABA and glycine immunoreactivity in the guinea pig superi- or olivary complex. Brain Res 501:269-286
  8. Hoffman DW, Hochreiter JS, Landry DR, Brimijoin MR, Tread- well MD, Gardner PD, Altschuler RA (1993) Localization of preproenkephalin mRNA-expressing cells in rat auditory brainstem with in situ hybridization. Hear Res 69:1-9
  9. Hökfelt T, Martensson R, Björklund A, Kleinau S, Goldstein M (1984) Distributional maps of tyrosine-hydroxylase-immuno- reactive neurons in the rat brain. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 2: classical transmitters in the CNS, part I. Elsevier Science, Amsterdam, pp 277-379
  10. Kungel M, Friauf E (1995) Somatostatin and leu-enkephalin in the rat auditory brainstem during fetal and postnatal development. Anat Embryol 191:425-443
  11. McLean IW, Nakane PK (1974) Periodate-lysine-paraformalde- hyde fixative. A new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077-1083
  12. Moore JK (1994) The human brainstem auditory pathway. In: Jackler RK, Brackmann DE (eds) Neurotology. Mosby, St. Louis, pp 1-17
  13. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordi- nates. 2nd edn. Academic Press, Sydney
  14. Puel JL (1995) Chemical synaptic transmission in the cochlea. Prog Neurobiol 47:449-476
  15. Ramsay H, House JR, Beattie JL, Moore JK (1996) A simple tech- nique for introducing anterograde and retrograde tracers into the vestibular and cochlear sensory organs. Acta Otolaryngol 116:39-43
  16. Rasmussen GL (1946) The olivary peduncle and other fiber pro- jections of the superior olivary complex. J Comp Neurol 84:141-219
  17. Riemann R, Reuss S (1998) Projection neurons in the superior oli- vary complex of the rat auditory brainstem: a double retro- grade tracing study. ORL 60:278-282
  18. Robertson D, Harvey AR, Cole KS (1989) Postnatal development of the efferent innervation of the rat cochlea. Dev Brain Res 47:197-207
  19. Safieddine S, Eybalin M (1992) Triple immunofluorescence evi- dence for the coexistence of acetylcholine, enkephalins and calcitonin gene-related peptide within efferent (olivocochlear) neurons of rats and guinea-pigs. Eur J Neurosci 4:981-992
  20. Saint Marie RL, Ostapoff EM, Morest DK, Wenthold RJ (1989) Glycine-immunoreactive projection of the cat lateral superior olive: possible role in mid-barin ear dominance. J Comp Neu- rol 279:382-396
  21. Schwartz IR (1992) The superior olivary complex and lateral lem- niscal nuclei. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: Neuroanatomy. Springer-Ver- lag, New York Berlin Heidelberg, pp 117-167
  22. Spangler KM, Warr WB (1991) The descending auditory system. In: Altschuler RA, Bobbin RP, Clopton BM, Hoffman DW (eds) Neurobiology of hearing: the central auditory system. Raven Press, New York, pp 27-45
  23. Strutz J (1981) Efferent innervation of the cochlea. Ann Otol Rhi- nol Laryngol 90:158-160
  24. Strutz J, Bielenberg K (1984) Efferent acoustic neurons within the lateral olivary nucleus of the guinea pig. Brain Res 299:174-177
  25. Vetter DE, Adams JC, Mugnaini E (1991) Chemically distinct rat olivocochlear neurons. Synapse 7:21-43
  26. 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 70:173-186
  27. Wang XY, Robertson D (1998) Substance P-induced inward cur- rent in identified auditory efferent neurons in rat brain stem slices. J Neurophysiol 80:218-229
  28. Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer-Ver- lag, New York Berlin Heidelberg, pp 410-448
  29. Warr WB, Beck JE (1996) Multiple projections from the ventral nucleus of the trapezoid body in the rat. Hear Res 93:83-101
  30. Webster WR (1995) Auditory system. In: Paxinos G (ed) The rat nervous system, 2nd edn. Academic Press, San Diego, pp 797-831
  31. White JS, Warr B (1983) The dual origins of the olivocochlear bundle in the albino rat. J Comp Neurol 219:203-214
  32. Wynne B, Robertson D (1997) Somatostatin and substance P-like immunoreactivity in the auditory brainstem of the adult rat. J Chem Neuroanat 12:259-266
  33. Wynne B, Harvey AR, Robertson D, Sirinathsinghji DJS (1995) Neurotransmitter and neuromodulator systems of the rat inferi- or colliculus and auditory brainstem studied by in situ hybrid- ization. J Chem Neuroanat 9:289-300
  34. Ylikoski J, Pirvola U, Häppölä O, Panula P, Virtanen I (1989) Im- munohistochemical demonstration of neuroactive substances in the inner ear of rat and guinea pig. Acta Otolaryngol Stock- holm 107:417-423