Advertisement

Identification of Inputs to Olivocochlear Neurons Using Transneuronal Labeling with Pseudorabies Virus (PRV)

  • M. Christian BrownEmail author
  • Sudeep Mukerji
  • Marie Drottar
  • Alanna M. Windsor
  • Daniel J. Lee
Research Article

Abstract

Olivocochlear (OC) neurons respond to sound and provide descending input that controls processing in the cochlea. The identities of neurons in the pathways providing inputs to OC neurons are incompletely understood. To explore these pathways, the retrograde transneuronal tracer pseudorabies virus (Bartha strain, expressing green fluorescent protein) was used to label OC neurons and their inputs in guinea pigs. Labeling of OC neurons began 1 day after injection into the cochlea. On day 2 (and for longer survival times), transneuronal labeling spread to the cochlear nucleus, inferior colliculus, and other brainstem areas. There was a correlation between the numbers of these transneuronally labeled neurons and the number of labeled medial (M) OC neurons, suggesting that the spread of labeling proceeds mainly via synapses on MOC neurons. In the cochlear nucleus, the transneuronally labeled neurons were multipolar cells including the subtype known as planar cells. In the central nucleus of the inferior colliculus, transneuronally labeled neurons were of two principal types: neurons with disc-shaped dendritic fields and neurons with dendrites in a stellate pattern. Transneuronal labeling was also observed in pyramidal cells in the auditory cortex and in centers not typically associated with the auditory pathway such as the pontine reticular formation, subcoerulean nucleus, and the pontine dorsal raphe. These data provide information on the identity of neurons providing input to OC neurons, which are located in auditory as well as non-auditory centers.

Keywords

superior olive cochlear nucleus inferior colliculus reflex pathway reticular formation 

Notes

Acknowledgments

This study was supported by NIH grants DCD 1 RO1 DC01089 (to MCB) and DCD 1 K08 DC06285 (to DJL). We thank Dr. L.W. Enquist (Princeton University) for generously providing the PRV 152 (supported by an NIH Virus Center Grant P40RR018604), Dr. Thane E. Benson for helping with the micrographs, and Dr. M. Charles Liberman for comments on a previous version of the manuscript. Preliminary results of this study were presented in abstract form at the Association for Research in Otolaryngology Midwinter Meeting, February, 2010.

References

  1. Arnesen AR (1984) Fibre population of the vestibulocochlear anastomosis in humans. Acta Otolaryngol 98:501–518Google Scholar
  2. Arnesen AR, Osen KK (1984) Fibre spectrum of the vestibulo-cochlear anastomosis in the cat. Acta Otolaryngol 98:255–269Google Scholar
  3. Aschoff A, Ostwald J (1987) Different origins of cochlear effernts in some bat species, rats, and guinea pigs. J Comp Neurol 264:56–72Google Scholar
  4. Benson TE, Brown MC (2006) Ultrastructure of synaptic input to medial olivocochlear neurons. J Comp Neurol 499:244–257PubMedCrossRefGoogle Scholar
  5. Billig I, Yeager MS, Blikas A, Raz Y (2007) Neurons in the cochlear nuclei controlling the tensor tympani in the rat: a study using pseudorabies virus. Brain Res 1154:124–136PubMedCrossRefGoogle Scholar
  6. 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
  7. Brown MC, de Venecia RK, Guinan JJ Jr (2003) Responses of medial olivocochlear (MOC) neurons: specifying the central pathways of the MOC reflex. Exp Brain Res 153:491–498PubMedCrossRefGoogle Scholar
  8. Brown MC, Lee DJ, Benson TE (2013a) Ultrastructure of spines and associated terminals on brainstem neurons controlling auditory input. Brain Res. doi: 10.1016/j.brainres.2013.04.020.
  9. Brown MC, Drottar M, Benson TE, Darrow KN (2013b) Commissural axons of the mouse cochlear nucleus. J Comp Neurol 521:1683–1696Google Scholar
  10. Card JP (2001) Pseudorabies virus neuroinvasiveness: a window into the functional organization of the brain. Adv Virus Res 56:39–71PubMedCrossRefGoogle Scholar
  11. Card JP, Levitt P, Enquist LW (1998) Different patterns of neuronal infection after intracerebral injection of two strains of pseudorabies virus. J Virol 75:4434–4441Google Scholar
  12. Contreras RJ, Gomez MM, Norgren R (1980) Central origins of cranial nerve parasympathetic neurons in the rat. J Comp Neurol 190:373–394PubMedCrossRefGoogle Scholar
  13. Darrow KN, Maison SF, Liberman MC (2006) Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 9:1474–1476PubMedCrossRefGoogle Scholar
  14. Darrow KN, Drottar M, Brown MC (2012) Planar multipolar cells in the cochlear nucleus project to medial olivocochlear neurons in mouse. J Comp Neurol 520:1365–1375PubMedCrossRefGoogle Scholar
  15. de Venecia RK, Liberman MC, Guinan JJ Jr, Brown MC (2005) Medial olivocochlear reflex interneurons are located in the posteroventral cochlear nucleus. J Comp Neurol 487:345–360PubMedCrossRefGoogle Scholar
  16. Delano P, Elgueda D, Hamame C, Robles L (2007) Selective attention to visual stimuli reduces cochlear sensitivity in chinchillas. J Neurosci 27:4146–4153PubMedCrossRefGoogle Scholar
  17. Doucet JR, Ryugo DK (1997) Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J Comp Neurol 385:245–264PubMedCrossRefGoogle Scholar
  18. Doucet JR, Ryugo DK (2006) Structural and functional classes of multipolar cells in the ventral cochlear nucleus. Anat Rec A 288A:331–344CrossRefGoogle Scholar
  19. Ekstrand MI, Enquist LW, Pomeranz LE (2008) The alpha-herpes viruses: molecular pathfinders in nervous system circuits. Trends Mol Med 14:134–140PubMedCrossRefGoogle Scholar
  20. Enquist LW, Card JP (2003) Recent advances in the use of neurotropic viruses for circuit analysis. Curr Opin Neurobiol 13:603–606PubMedCrossRefGoogle Scholar
  21. Faye-Lund H (1986) Projection from the inferior colliculus to the superior olivary complex in the albino rat. Anat Embryol 175:35–52PubMedCrossRefGoogle Scholar
  22. Godfrey DA, Kiang NYS, Norris BE (1975) Single unit activity in the posteroventral cochlear nucleus of the cat. J Comp Neurol 162:247–268PubMedCrossRefGoogle Scholar
  23. Groff A, Liberman MC (2003) Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. J Neurophysiol 90:3178–3200PubMedCrossRefGoogle Scholar
  24. Guinan JJ Jr, Warr WB, Norris BE (1984) Topographic organization of the olivocochlear projections from the lateral and medial zones of the superior olivary complex. J Comp Neurol 226:21–27PubMedCrossRefGoogle Scholar
  25. Hackney CM, Osen KK, Kolston J (1990) Anatomy of the cochlear nuclear complex of the guinea pig. Anat Embryol 182:123–149PubMedCrossRefGoogle Scholar
  26. Horvath M, Ribari O, Repassy G, Toth IE, Boldogkoi Z, Palkovits M (2003) Intracochlear injection of pseudorabies virus labels descending auditory and monoaminerg projections to olivocochlear cells in guinea pig. Eur J Neurosci 18:1439–1447PubMedCrossRefGoogle Scholar
  27. Hurley PA, Clarke M, Crook JM, Wis AK, Shepherd RK (2003) Cochlear immunochemistry—a new technique based on gelatin embedding. J Neurosci Meth 129:81–86CrossRefGoogle Scholar
  28. Liberman MC (1988) Response properties of cochlear efferent neurons: monaural vs. binaural stimulation and the effects of noise. J Neurophysiol 60:1779–1798PubMedGoogle Scholar
  29. Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17–36PubMedCrossRefGoogle Scholar
  30. Liberman MC, Guinan JJ Jr (1998) Feedback control of the auditory periphery: anti-masking effects of middle ear muscles vs. olivocochlear efferents. J Commun Disord 31:471–483PubMedCrossRefGoogle Scholar
  31. Loftus WC, Malmierca MS, Bishop DC, Oliver DL (2008) The cytoarchitecture of the inferior colliculus revisited: a common organization of the lateral cortex in rat and cat. Neuroscience 154:196–205PubMedCrossRefGoogle Scholar
  32. Malmierca MS, Blackstad TW, Osen KK, Karagulle T, Molowny RL (1993) The central nucleus of the inferior colliculus in rat: a Golgi and computer reconstruction study of neuronal and laminar structure. J Comp Neurol 333:1–27PubMedCrossRefGoogle Scholar
  33. Mesulam MM (1982) Principles of horseradish peroxidase neurohistochemistry and their applications for tracing neural pathways—axonal transport, enzyme histochemistry and light microscopic analysis. In: Mesulam M-M (ed) Tracing neural connections with horseradish peroxidase. Wiley, Chichester, pp 1–151Google Scholar
  34. Mukerji S, Windsor AM, Lee DJ (2010) Auditory brainstem circuits that mediate the middle ear muscle reflex. Trends Amplif 14:170–191PubMedCrossRefGoogle Scholar
  35. Mulders WHAM, Robertson D (2000a) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hear Res 144:65–72PubMedCrossRefGoogle Scholar
  36. Mulders WHAM, Robertson D (2000b) Morphological relationships of peptidergic and noradrenergic nerve terminals to olivocochlear neurones in the rat. Hear Res 144:53–64PubMedCrossRefGoogle Scholar
  37. Mulders WHAM, Robertson D (2001) Origin of the noradrenergic innervation of the superior olivary complex in the rat. J Chem Neuroanat 21:313–322PubMedCrossRefGoogle Scholar
  38. Mulders WHAM, Robertson D (2005a) Noradrenergic modulation of brainstem nuclei alters cochlear neural output. Hear Res 204:147–155PubMedCrossRefGoogle Scholar
  39. Mulders WHAM, Robertson D (2005b) Catecholaminergic innervation of guinea pig superior olivary complex. J Chem Neuroanat 30:230–242PubMedCrossRefGoogle Scholar
  40. O-Donnell P, Lavin A, Enquist LW, Grace AA, Card JP (1997) Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. J Neurosci 17:2143–2167Google Scholar
  41. Oliver DL, Huerta MF (1992) Inferior and superior colliculi. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 168–221CrossRefGoogle Scholar
  42. Oliver DL, Morest DK (1984) The central nucleus of the inferior colliculus in the cat. J Comp Neurol 222:237–264PubMedCrossRefGoogle Scholar
  43. Oliver DL, Kuwada S, Yin TCT, Haberly LB, Henkel CK (1991) Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J Comp Neurol 303:75–100PubMedCrossRefGoogle Scholar
  44. Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–484PubMedCrossRefGoogle Scholar
  45. Ota Y, Oliver DL, Dolan DF (2004) Frequency specific effects on cochlear responses during activation of the inferior colliculus in the guinea pig. J Neurophysiol 91:2185–2193PubMedCrossRefGoogle Scholar
  46. Pagano M, Gauvreau K (2000) Principles of biostatistics, 2nd edn. Duxbury, Pacific GroveGoogle Scholar
  47. Pickard GE, Smeraski CA, Tomlinson CC, Banfield BW, Kaufman J, Wilcox CL, Enquist LW, Sollars PJ (2002) Intravitreal injection of the attenuated Pseudorabies virus PRV Bartha in infection of the hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits. J Neurosci 22:2701–2710Google Scholar
  48. Robertson D (1984) Horseradish peroxidase injection of physiologically characterized afferent and efferent neurons in the guinea pig spiral ganglion. Hear Res 15:113–121PubMedCrossRefGoogle Scholar
  49. Ryugo DK, Fay RR, Popper AN (2011) Auditory and vestibular efferents, vol 38. Springer, New YorkCrossRefGoogle Scholar
  50. Smith BN, Banfield BW, Smeraski CA, Wilcox CL, Dudek FE, Enquist LW, Pickard GE (2000) Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc Natl Acad Sci USA 97:9264–9269Google Scholar
  51. Spangler KM, Henkel CK, Miller IJ Jr (1982) Localization of the motor neurons to the tensor tympani muscle. Neurosci Lett 32:23–27PubMedCrossRefGoogle Scholar
  52. Strutz J (1982) The origin of efferent innervation vestibular fibers in the guinea pig. Acta Otolaryngol 94:299–305PubMedCrossRefGoogle Scholar
  53. Strutz J, Bielenberg K (1984) Efferent acoustic neurons within the lateral superior olivary nucleus of the guinea pig. Brain Res 299:174–177PubMedCrossRefGoogle Scholar
  54. Thompson AM, Thompson GC (1991) Posteroventral cochlear nucleus projections to olivocochlear neurons. J Comp Neurol 303:267–285PubMedCrossRefGoogle Scholar
  55. Thompson AM, Thompson GC (1993) Relationship of descending inferior colliculus projections to olivocochlear neurons. J Comp Neurol 335:402–412PubMedCrossRefGoogle Scholar
  56. Thompson AM, Thompson GC (1995) Light microscopic evidence of serotoninergic projections to olivocochlear neurons in the bush baby (Otolemur garnettii). Brain Res 695:263–266PubMedCrossRefGoogle Scholar
  57. 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 185:1–16PubMedCrossRefGoogle Scholar
  58. 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 70:173–186PubMedCrossRefGoogle Scholar
  59. Warr WB (1969) Fiber degeneration following lesions in the posteroventral cochlear nucleus of the cat. Exp Neurol 23:140–155PubMedCrossRefGoogle Scholar
  60. Windsor A, Roska B, Brown MC, Lee DJ (2007) Transneuronal analysis of the middle ear muscle reflex pathways using pseudorabies virus. Abstr Assoc Res Otolaryngol, #605Google Scholar
  61. Winer JA (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 222–409CrossRefGoogle Scholar
  62. Woods CI, Azeredo WJ (1999) Noradrenergic and serotonergic projections to the superior olive: potential for modulation of olivocochlear neuron. Brain Res 836:9–18PubMedCrossRefGoogle Scholar
  63. 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 420:127–138PubMedCrossRefGoogle Scholar

Copyright information

© Association for Research in Otolaryngology 2013

Authors and Affiliations

  • M. Christian Brown
    • 1
    • 2
    Email author
  • Sudeep Mukerji
    • 1
  • Marie Drottar
    • 1
  • Alanna M. Windsor
    • 1
  • Daniel J. Lee
    • 1
    • 2
  1. 1.Eaton-Peabody LaboratoryMassachusetts Eye and Ear InfirmaryBostonUSA
  2. 2.Department of Otology and LaryngologyHarvard Medical SchoolBostonUSA

Personalised recommendations