Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Jul 15;89(14):6324–6327. doi: 10.1073/pnas.89.14.6324

Developmental segregation in the afferent projections to mammalian auditory hair cells.

S M Echteler 1
PMCID: PMC49493  PMID: 1631126

Abstract

The mammalian ear contains two types of auditory receptors, inner and outer hair cells, that lie in close proximity to each other within the sensory epithelium of the cochlea. In adult mammals, these two classes of auditory hair cells are innervated by separate populations of afferent neurons that differ strikingly in their cellular morphology and their pattern of arborization within the cochlea. At present, it is unclear when or how these distinctive patterns of cochlear innervation emerge and become segregated during development. In the present study, an in vitro horseradish peroxidase labeling method was used to examine the formation of individual auditory neuron arbors at the same location within the apex of the developing gerbil cochlea. At birth, most cochlear neurons displayed peripheral arbors that embraced both inner and outer hair cell receptors. During the next 6 days, however, the arbors of individual cochlear afferents become confined to either the inner or outer hair cell zone, and thus there is a complete segregation of afferent innervation. This neural segregation occurs principally through the withdrawal of inappropriate connections to the outer hair cell system and is completed well before hearing commences.

Full text

PDF
6324

Images in this article

6325Image
on p.6325
6325Image
on p.6325

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams J. C. Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem. 1981 Jun;29(6):775–775. doi: 10.1177/29.6.7252134. [DOI] [PubMed] [Google Scholar]
  2. Berglund A. M., Ryugo D. K. Hair cell innervation by spiral ganglion neurons in the mouse. J Comp Neurol. 1987 Jan 22;255(4):560–570. doi: 10.1002/cne.902550408. [DOI] [PubMed] [Google Scholar]
  3. Brown M. C. Morphology of labeled afferent fibers in the guinea pig cochlea. J Comp Neurol. 1987 Jun 22;260(4):591–604. doi: 10.1002/cne.902600411. [DOI] [PubMed] [Google Scholar]
  4. Burda H., Branis M. Postnatal development of the organ of Corti in the wild house mouse, laboratory mouse, and their hybrid. Hear Res. 1988 Oct;36(1):97–105. doi: 10.1016/0378-5955(88)90140-2. [DOI] [PubMed] [Google Scholar]
  5. Carlier E., Abonnenc M., Pujol R. Maturation des réponses unitaires à la stimulation tonale dans le nerf cocléaire du chaton. J Physiol (Paris) 1975 Jul;70(2):129–138. [PubMed] [Google Scholar]
  6. Cole K. S., Robertson D. Early efferent innervation of the developing rat cochlea studied with a carbocyanine dye. Brain Res. 1992 Mar 20;575(2):223–230. doi: 10.1016/0006-8993(92)90083-l. [DOI] [PubMed] [Google Scholar]
  7. Echteler S. M., Arjmand E., Dallos P. Developmental alterations in the frequency map of the mammalian cochlea. Nature. 1989 Sep 14;341(6238):147–149. doi: 10.1038/341147a0. [DOI] [PubMed] [Google Scholar]
  8. Emmerling M. R., Sobkowicz H. M., Levenick C. V., Scott G. L., Slapnick S. M., Rose J. E. Biochemical and morphological differentiation of acetylcholinesterase-positive efferent fibers in the mouse cochlea. J Electron Microsc Tech. 1990 Jun;15(2):123–143. doi: 10.1002/jemt.1060150205. [DOI] [PubMed] [Google Scholar]
  9. Ginzberg R. D., Morest D. K. A study of cochlear innervation in the young cat with the Golgi method. Hear Res. 1983 May;10(2):227–246. doi: 10.1016/0378-5955(83)90056-4. [DOI] [PubMed] [Google Scholar]
  10. Horner K. C., Serviere J., Granier-Deferre C. Deoxyglucose demonstration of in-utero hearing in the guinea pig foetus. Hear Res. 1987;26(3):327–333. doi: 10.1016/0378-5955(87)90068-2. [DOI] [PubMed] [Google Scholar]
  11. Kiang N. Y., Rho J. M., Northrop C. C., Liberman M. C., Ryugo D. K. Hair-cell innervation by spiral ganglion cells in adult cats. Science. 1982 Jul 9;217(4555):175–177. doi: 10.1126/science.7089553. [DOI] [PubMed] [Google Scholar]
  12. Kikuchi K., Hilding D. The development of the organ of Corti in the mouse. Acta Otolaryngol. 1965 Sep;60(3):207–222. doi: 10.3109/00016486509127003. [DOI] [PubMed] [Google Scholar]
  13. Lenoir M., Shnerson A., Pujol R. Cochlear receptor development in the rat with emphasis on synaptogenesis. Anat Embryol (Berl) 1980;160(3):253–262. doi: 10.1007/BF00305106. [DOI] [PubMed] [Google Scholar]
  14. Morey A. L., Carlile S. Auditory brainstem of the ferret: maturation of the brainstem auditory evoked response. Brain Res Dev Brain Res. 1990 Mar 1;52(1-2):279–288. doi: 10.1016/0165-3806(90)90246-u. [DOI] [PubMed] [Google Scholar]
  15. Nakai Y., Hilding D. Cochlear development. Some electron microscopic observations of maturation of hair cells, spiral ganglion and Reissner's membrane. Acta Otolaryngol. 1968 Nov;66(5):369–385. doi: 10.3109/00016486809126303. [DOI] [PubMed] [Google Scholar]
  16. Perkins R. E., Morest D. K. A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarkski Optics. J Comp Neurol. 1975 Sep 15;163(2):129–158. doi: 10.1002/cne.901630202. [DOI] [PubMed] [Google Scholar]
  17. Pujol R., Abonnenc M. Receptor maturation and synaptogenesis in the golden hamster cochlea. Arch Otorhinolaryngol. 1977 Jun 30;217(1):1–12. doi: 10.1007/BF00453886. [DOI] [PubMed] [Google Scholar]
  18. Pujol R., Carlier E. Cochlear synaptogenesis after sectioning the efferent bundle. Brain Res. 1982 Jan;255(1):151–154. doi: 10.1016/0165-3806(82)90084-0. [DOI] [PubMed] [Google Scholar]
  19. Pujol R., Carlier E., Devigne C. Different patterns of cochlear innervation during the development of the kitten. J Comp Neurol. 1978 Feb 1;177(3):529–536. doi: 10.1002/cne.901770311. [DOI] [PubMed] [Google Scholar]
  20. Rogers S. L., Letourneau P. C., Pech I. V. The role of fibronectin in neural development. Dev Neurosci. 1989;11(4-5):248–265. doi: 10.1159/000111904. [DOI] [PubMed] [Google Scholar]
  21. Ruben R. J. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol. 1967;(Suppl):1–44. [PubMed] [Google Scholar]
  22. SPOENDLIN H. H., GACEK R. R. ELECTRON MICROSCOPIC STUDY OF THE EFFERENT AND AFFERENT INNERVATION OF THE ORGAN OF CORTI IN THE CAT. Ann Otol Rhinol Laryngol. 1963 Sep;72:660–686. doi: 10.1177/000348946307200307. [DOI] [PubMed] [Google Scholar]
  23. Schmiedt R. A., Zwislocki J. J. Comparison of sound-transmission and cochlear-microphonic characteristics in Mongolian gerbil and guinea pig. J Acoust Soc Am. 1977 Jan;61(1):133–149. doi: 10.1121/1.381283. [DOI] [PubMed] [Google Scholar]
  24. Simmons D. D., Liberman M. C. Afferent innervation of outer hair cells in adult cats: I. Light microscopic analysis of fibers labeled with horseradish peroxidase. J Comp Neurol. 1988 Apr 1;270(1):132–144. doi: 10.1002/cne.902700111. [DOI] [PubMed] [Google Scholar]
  25. Simmons D. D., Manson-Gieseke L., Hendrix T. W., McCarter S. Reconstructions of efferent fibers in the postnatal hamster cochlea. Hear Res. 1990 Nov;49(1-3):127–139. doi: 10.1016/0378-5955(90)90100-4. [DOI] [PubMed] [Google Scholar]
  26. Simmons D. D., Manson-Gieseke L., Hendrix T. W., Morris K., Williams S. J. Postnatal maturation of spiral ganglion neurons: a horseradish peroxidase study. Hear Res. 1991 Sep;55(1):81–91. doi: 10.1016/0378-5955(91)90094-p. [DOI] [PubMed] [Google Scholar]
  27. Sobkowicz H. M., Emmerling M. R. Development of acetylcholinesterase-positive neuronal pathways in the cochlea of the mouse. J Neurocytol. 1989 Apr;18(2):209–224. doi: 10.1007/BF01206663. [DOI] [PubMed] [Google Scholar]
  28. Sobkowicz H. M., Rose J. E., Scott G. E., Slapnick S. M. Ribbon synapses in the developing intact and cultured organ of Corti in the mouse. J Neurosci. 1982 Jul;2(7):942–957. doi: 10.1523/JNEUROSCI.02-07-00942.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sobkowicz H. M., Rose J. E., Scott G. L., Levenick C. V. Distribution of synaptic ribbons in the developing organ of Corti. J Neurocytol. 1986 Dec;15(6):693–714. doi: 10.1007/BF01625188. [DOI] [PubMed] [Google Scholar]
  30. Spoendlin H. Innervation densities of the cochlea. Acta Otolaryngol. 1972 Feb-Mar;73(2):235–248. doi: 10.3109/00016487209138937. [DOI] [PubMed] [Google Scholar]
  31. Spoendlin H. Innervation patterns in the organ of corti of the cat. Acta Otolaryngol. 1969 Feb-Mar;67(2):239–254. doi: 10.3109/00016486909125448. [DOI] [PubMed] [Google Scholar]
  32. Woolf N. K., Koehrn F. J., Ryan A. F. Immunohistochemical localization of fibronectin-like protein in the inner ear of the developing gerbil and rat. Brain Res Dev Brain Res. 1992 Jan 17;65(1):21–33. doi: 10.1016/0165-3806(92)90004-g. [DOI] [PubMed] [Google Scholar]
  33. Woolf N. K., Ryan A. F. The development of auditory function in the cochlea of the mongolian gerbil. Hear Res. 1984 Mar;13(3):277–283. doi: 10.1016/0378-5955(84)90081-9. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES