Experimental Brain Research

, Volume 153, Issue 4, pp 491–498

Responses of medial olivocochlear neurons

Specifying the central pathways of the medial olivocochlear reflex
  • M. C. Brown
  • R. K. de Venecia
  • J. J. GuinanJr
Research Article

Abstract

Medial olivocochlear (MOC) neurons project to outer hair cells (OHC), forming the efferent arm of a reflex that affects sound processing and offers protection from acoustic overstimulation. The central pathways that trigger the MOC reflex in response to sound are poorly understood. Insight into these pathways can be obtained by examining the responses of single MOC neurons recorded from anesthetized guinea pigs. Response latencies of MOC neurons are as short as 5 ms. This latency is consistent with the idea that type I, but not type II, auditory-nerve fibers provide the major inputs to the reflex interneurons in the cochlear nucleus. This short latency also implies that the cochlear-nucleus interneurons have rapidly conducting axons. In the cochlear nucleus, lesions of the posteroventral subdivision (PVCN), but not the anteroventral (AVCN) or dorsal (DCN) subdivisions, produce permanent disruption of the MOC reflex, based on a metric of adaptation of the distortion-product otoacoustic emission (DPOAE). This finding supports earlier anatomical results demonstrating that some PVCN neurons project to MOC neurons. Within the PVCN, there are two general types of units when classified according to poststimulus time histograms: onset units and chopper units. The MOC response is sustained and cannot be produced solely by inputs having an onset pattern. The MOC reflex interneurons are thus likely to be chopper units of PVCN. Also supporting this conclusion, chopper units and MOC neurons both have sharp frequency tuning. Thus, the most likely pathway for the sound-evoked MOC reflex begins with the responses of hair cells, proceeds with type I auditory-nerve fibers, PVCN chopper units, and MOC neurons, and ends with the MOC terminations on OHC.

Keywords

Interneuron Cochlea Outer hair cell Cochlear nucleus Auditory nerve 

References

  1. Adams JC (1996) Axon terminals on olivocochlear neurons. Soc Neurosci Abstr 22:127Google Scholar
  2. Borg E (1973) On the neuronal organization of the acoustic middle ear reflex. A physiological and anatomical study. Brain Res 49:101–123CrossRefPubMedGoogle Scholar
  3. Boyev K, Liberman M, Brown M (2002) Effects of anesthesia on efferent-mediated adaptation of the DPOAE. J Assoc Res Otolaryngol 3:362–373Google Scholar
  4. Brawer JR, Morest DK, Kane EC (1974) The neuronal architecture of the cochlear nucleus of the cat. J Comp Neurol 155:251–300PubMedGoogle Scholar
  5. Brown MC (1989) Morphology and response properties of single olivocochlear fibers in the guinea pig. Hearing Res 40:93–110CrossRefGoogle Scholar
  6. Brown MC (1993) Anatomical and physiological studies of type I and type II spiral ganglion neurons. In: Merchan MA, Juiz JM, Godfrey DA, Mugnaini E (eds) The mammalian cochlear nuclei: organization and function. Plenum, New York, pp 43–54Google Scholar
  7. Brown MC (1994) Antidromic responses of single units from the spiral ganglion. J Neurophysiol 71:1835–1847PubMedGoogle Scholar
  8. Brown MC (2001) Response adaptation of medial olivocochlear neurons is minimal. J Neurophysiol 86:2381–2392PubMedGoogle Scholar
  9. Brown MC, Kujawa SG, Duca ML (1998) Single olivocochlear neurons in the guinea pig. I. Binaural facilitation of responses to high-level noise. J Neurophysiol 79:3077–3087PubMedGoogle Scholar
  10. Cant NB, Gaston KC (1982) Pathways connecting the right and left cochlear nuclei. J Comp Neurol 212:313–326PubMedGoogle Scholar
  11. de Venecia RK, Liberman MC, Guinan JJ Jr, Brown MC (2001) Effects of kainate lesions in different cochlear nucleus regions on the MOC reflex. Abstr Assoc Res Otolaryngol 46Google Scholar
  12. Doucet JR, Ryugo DK (2002) Projections of multipolar neurons in the ventral cochlear nucleus to the lateral superior olive in rats. Abstr Assoc Res OtolaryngolGoogle Scholar
  13. Evans EF (1972) The frequency response and other properties of single fibres in the guinea-pig cochlear nerve. J Physiol (Lond) 226:263–287Google Scholar
  14. Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol 175:35–52PubMedGoogle Scholar
  15. Fekete DM, Rouiller EM, Liberman MC, Ryugo DK (1984) The central projections of intracellularly labeled auditory nerve fibers in cats. J Comp Neurol 229:432–450PubMedGoogle Scholar
  16. Fex J (1962) Auditory activity in centrifugal and centripetal cochlear fibers in cat. Acta Physiol Scand 55: S1891–68Google Scholar
  17. Fex J (1965) Auditory activity in uncrossed centrifugal cochlear fibers in cat. Acta Physiol Scand 64:43–57Google Scholar
  18. Friauf E, Ostwald J (1988) Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase. Exp Brain Res 73:263–284PubMedGoogle Scholar
  19. Godfrey DA, Kiang NYS, Norris BE (1975) Single unit activity in the posteroventral cochlear nucleus of the cat. J Comp Neurol 162:247–268PubMedGoogle Scholar
  20. Guinan JJ Jr (1996) The physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RR (eds) The cochlea. Springer, New York, pp 435–502Google Scholar
  21. Guinan JJ Jr, Gifford ML (1988) Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. I. Rate-level functions. Hearing Res 33:97–114CrossRefGoogle Scholar
  22. Gummer M, Yates GK, Johnstone BM (1988) Modulation transfer functions of efferent neurones in the guinea pig cochlea. Hearing Res 36:41–52CrossRefGoogle Scholar
  23. Hackney CM, Osen KK, Kolston J (1990) Anatomy of the cochlear nuclear complex of the guinea pig. Anat Embryol 182:123–149PubMedGoogle Scholar
  24. Ito J, Honjo I (1988) Electrophysiological and HRP studies of the direct afferent inputs from the cochlear nuclei to the tensor tympani muscle motoneurons in the cat. Acta Otolaryngol 105:292–296PubMedGoogle Scholar
  25. Itoh K, Nomura S, Konishi A, Yasui Y, Sugimoto T, Muzion N (1986) A morphological evidence of direct connections from the cochlear nuclei to tensor tympani motoneurons in the cat: a possible afferent limb of the acoustic middle ear reflex pathways. Brain Res 375:214–219CrossRefPubMedGoogle Scholar
  26. Jiang D, Palmer AR, Winter IM (1996) Frequency extent of two-tone facilitation in onset units in the ventral cochlear nucleus. J Neurophysiol 75:380–395PubMedGoogle Scholar
  27. Kawase T, Delgutte B, Liberman MC (1993) Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. J Neurophysiol 70:2533–2549PubMedGoogle Scholar
  28. Kiang NYS, Rho JM, Northrop CC, Liberman MC, Ryugo DK (1982) Hair-cell innervation by spiral ganglion cells in adult cats. Science 217:175–177PubMedGoogle Scholar
  29. Kim DO (1986) Active and nonlinear cochlear biomechanics and the role of outer-hair-cell subsystem in the mammalian auditory system. Hearing Res 22:105–114CrossRefGoogle Scholar
  30. Kobler JB, Vacher SR, Guinan JJ Jr (1987) The recruitment order of stapedius motoneurons in the acoustic reflex varies with sound laterality. Brain Res 425:372–375CrossRefPubMedGoogle Scholar
  31. Kobler JB, Guinan JJ Jr, Vacher SR, Norris BE (1992) Acoustic reflex frequency selectivity in single stapedius motoneurons of the cat. J Neurophysiol 68:807–817PubMedGoogle Scholar
  32. Kujawa S, Liberman MC (2001) Effects of olivocochlear feedback on distortion product otoacoustic emissions in guinea pig. J Assoc Res Otolaryngol 2:268–278PubMedGoogle Scholar
  33. Liberman MC (1988) Response properties of cochlear efferent neurons: Monaural vs binaural stimulation and the effects of noise. J Neurophysiol 60:1779–1798PubMedGoogle Scholar
  34. Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hearing Res 24:17–36CrossRefGoogle Scholar
  35. Liberman MC, Puria S, Guinan JJ Jr (1996) The ipsilaterally evoked olivocochlear reflex causes rapid adaptation of the 2f1–f2 distortion product otoacoustic emission. J Acoust Soc Am 99:3572–3584PubMedGoogle Scholar
  36. McCue MP, Guinan JJ Jr (1988) Anatomical and functional segregation in the stapedius motoneuron pool of the cat. J Neurophysiol 60:1160–1180PubMedGoogle Scholar
  37. Melcher JR, Knudson IM, Fullerton BC, Guinan JJ Jr, Norris BE, Kiang NYS (1996) Generators of the brainstem auditory evoked potential in cat I: An experimental approach to their identification. Hearing Res 93:1-27CrossRefGoogle Scholar
  38. Mugnaini E, Warr WB, Osen KK (1980) Distribution and light microscopic features of granule cells in the cochlear nucleus of cat, rat, and mouse. J Comp Neurol 191:581–606PubMedGoogle Scholar
  39. Mulders WHAM, Robertson D (2000a) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hearing Res 144:65–72CrossRefGoogle Scholar
  40. Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–484PubMedGoogle Scholar
  41. Rajan R (1988) Effect of electrical stimulation of the crossed olivocochlear bundle on temporary threshold shifts in auditory sensitivity. I. Dependence on electrical stimulation parameters. J Neurophysiol 60:549–568PubMedGoogle Scholar
  42. Reiter ER, Liberman MC (1995) Efferent mediated protection from acoustic overexposure: relation to “slow” effects of olivocochlear stimulation. J Neurophysiol 73:506–514PubMedGoogle Scholar
  43. Rhode WS, Greenberg S (1992) Physiology of the cochlear nuclei. In: Popper AN, Fay RR (eds) The mammalian auditory pathway: neurophysiology. Springer, New York, pp 94–152Google Scholar
  44. Rhode WS, Oertel D, Smith PH (1983) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. J Comp Neurol 213:448–463PubMedGoogle Scholar
  45. Rhode WW, Kettner RE (1987) Physiological study of neurons in the dorsal and posteroventral cochlear nucleus of the unanesthetized cat. J Neurophysiol 57:414–442PubMedGoogle Scholar
  46. Robertson D (1984) Horseradish peroxidase injection of physiologically characterized afferent and efferent neurons in the guinea pig spiral ganglion. Hearing Res 15:113–121CrossRefGoogle Scholar
  47. Robertson D, Gummer M (1985) Physiological and morphological characterization of efferent neurons in the guinea pig cochlea. Hearing Res 20:63–77CrossRefGoogle Scholar
  48. Robertson D, Winter IM (1988) Cochlear nucleus inputs to olivocochlear neurones revealed by combined anterograde and retrograde labelling in the guinea pig. Brain Res 462:47–55CrossRefPubMedGoogle Scholar
  49. Robertson D, Sellick PM, Patuzzi R (1999) The continuing search for outer hair cell afferents in the guinea pig spiral ganglion. Hearing Res 136:151–158CrossRefGoogle Scholar
  50. Rouiller EM, Ryugo DK (1984) Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J Comp Neurol 225:167–186PubMedGoogle Scholar
  51. Rouiller EM, Capt M, Dolivo M, Ribaupierre F de (1986) Tensor tympani reflex pathways studied with retrograde horseradish peroxidase and transneuronal viral tracing techniques. Neurosci Lett 72:247–252CrossRefPubMedGoogle Scholar
  52. Schofield BR, Cant NB (1996) Origins and targets of commissural connections between the cochlear nuclei in guinea pigs. J Comp Neurol 375:128–146CrossRefPubMedGoogle Scholar
  53. Spoendlin H (1971) Degeneration behaviour of the cochlear nerve. Arch Klin Exp Ohren Nasen Kehlkopfheilkd 200:275–291PubMedGoogle Scholar
  54. Thompson AM, Thompson GC (1991) Posteroventral cochlear nucleus projections to olivocochlear neurons. J Comp Neurol 303:267–285PubMedGoogle Scholar
  55. Vacher SR, Guinan JJ Jr, Kober JB (1989) Intracellularly labeled stapedius-motoneuron cell bodies in the cat are spatially organized according to their physiologic responses. J Comp Neurol 289:401–415PubMedGoogle Scholar
  56. Warr WB (1969) Fiber degeneration following lesions in the posteroventral cochlear nucleus of the cat. Exp Neurol 23:140–155PubMedGoogle Scholar
  57. Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 410–448Google Scholar
  58. Wenthold RJ (1987) Evidence for a glycinergic pathway connecting the two cochlear nuclei: an immunohistochemical and retrograde transport study. Brain Res 415:183–187CrossRefPubMedGoogle Scholar
  59. Wiederhold ML, Kiang NYS (1970) Effects of electric stimulation of the crossed olivocochlear bundle on single auditory-nerve fibers in the cat. J Acoust Soc Am 48:950–965PubMedGoogle Scholar
  60. Winslow R, Sachs MB (1987) Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. J Neurophysiol 57:1002–1021PubMedGoogle Scholar
  61. 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 420:127–138CrossRefPubMedGoogle Scholar
  62. Young ED, Robert J-M, Shofner WP (1988) Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. J Neurophysiol 60:1-29PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • M. C. Brown
    • 1
    • 2
  • R. K. de Venecia
    • 1
    • 2
  • J. J. GuinanJr
    • 1
    • 2
  1. 1.Department of Otology and LaryngologyHarvard Medical SchoolUSA
  2. 2.Eaton-Peabody LaboratoryMassachusetts Eye & Ear InfirmaryBostonUSA

Personalised recommendations