Urocortin-expressing olivocochlear neurons exhibit tonotopic and developmental changes in the auditory brainstem and in the innervation of the cochlea

Journal of Comparative Neurology

Volumn 519, Issue 14, 2011, Pages 2758-2778

  Kaiser, Alexander ^a   Alexandrova, Olga ^a   Grothe, Benedikt ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Auditory brainstem; Cochlea; Cochlear efferents; Development; Hearing onset; Inner hair cells; Lateral olivocochlear neurons; Stress and hearing; Tinnitus; Urocortin

Indexed keywords

UROCORTIN; UROCORTIN II; UROCORTIN III;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; AUDITORY SYSTEM; BRAIN STEM; CELL DENSITY; CHOLINERGIC NERVE CELL; COCHLEA; CONTROLLED STUDY; FEMALE; GERBIL; IMMUNOASSAY; IMMUNOHISTOLOGY; IMMUNOREACTIVITY; MALE; MYELINATION; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; OLIVOCOCHLEAR NEURON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPERIOR OLIVARY NUCLEUS; SURVIVAL TIME; SYNAPSE;

ACETYLCHOLINE; ANIMALS; BRAIN STEM; COCHLEA; FEMALE; GERBILLINAE; HAIR CELLS, AUDITORY, INNER; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; OLIVARY NUCLEUS; SYNAPSES; UROCORTINS;

EID: 79960782501     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22650     Document Type: Article

References (65)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94: 239-247.
2. Al Mana D, Ceranic B, Djahanbakhch O, Luxon LM. 2008. Hormones and the auditory system: a review of physiology and pathophysiology. Neuroscience 153: 881-900.
3. Altschuler RA, Kachar B, Rubio JA, Parakkal MH, Fex J. 1985. Immunocytochemical localization of choline acetyltransferase-like immunoreactivity in the guinea pig cochlea. Brain Res 338: 1-11.
4. Bajjalieh SM, Peterson K, Shinghal R, Scheller RH. 1992. SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257: 1271-1273.
5. Ban JH, Jin SM. 2006. A clinical analysis of psychogenic sudden deafness. Otolaryngol Head Neck Surg 134: 970-974.
6. Bittencourt JC, Vaughan J, Arias C, Rissman RA, Vale WW, Sawchenko PE. 1999. Urocortin expression in rat brain: evidence against a pervasive relationship of urocortin-containing projections with targets bearing type 2 CRF receptors. J Comp Neurol 415: 285-312.
7. Canlon B, Meltser I, Johansson P, Tahera Y. 2007. Glucocorticoid receptors modulate auditory sensitivity to acoustic trauma. Hear Res 226: 61-69.
8. Darrow KN, Maison SF, Liberman MC. 2006. Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 9: 1474-1476.
9. De Kloet ER, Joels M, Holsboer F. 2005. Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6: 463-475.
10. Dechesne CJ, Rabejac D, Desmadryl G. 1994. Development of calretinin immunoreactivity in the mouse inner ear. J Comp Neurol 346: 517-529.
11. Eybalin M. 1993. Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol Rev 73: 309-373.
12. Fagelson MA. 2007. The association between tinnitus and posttraumatic stress disorder. Am J Audiol 16: 107-117.
13. Feany MB, Lee S, Edwards RH, Buckley KM. 1992. The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70: 861-867.
14. Gaszner B, Jensen KO, Farkas J, Reglodi D, Csernus V, Roubos EW, Kozicz T. 2009. Effects of maternal separation on dynamics of urocortin 1 and brain-derived neurotrophic factor in the rat non-preganglionic Edinger-Westphal nucleus. Int J Dev Neurosci 27: 439-451.
15. German DC, Bruce G, Hersh LB. 1985. Immunohistochemical staining of cholinergic neurons in the human brain using a polyclonal antibody to human choline acetyltransferase. Neurosci Lett 61: 1-5.
16. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447: 1-7.
17. Guinan JJ Jr. 1996. The physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RF, editors. Springer handbook of auditory research: the cochlea, 1st ed. New York: Springer Verlag. p 435-502.
18. Hebert S, Lupien SJ. 2007. The sound of stress: blunted cortisol reactivity to psychosocial stress in tinnitus sufferers. Neurosci Lett 411: 138-142.
19. Heinrichs SC, Koob GF. 2004. Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J Pharmacol Exp Ther 311: 427-440.
20. Helfert RH, Juiz JM, Bledsoe SC Jr, Bonneau JM, Wenthold RJ, Altschuler RA. 1992. Patterns of glutamate, glycine, and GABA immunolabeling in four synaptic terminal classes in the lateral superior olive of the guinea pig. J Comp Neurol 323: 305-325.
21. Henkel CK, Brunso-Bechtold JK. 1998. Calcium-binding proteins and GABA reveal spatial segregation of cell types within the developing lateral superior olivary nucleus of the ferret. Microsc Res Tech 41: 234-245.
22. Hinton DE, Chhean D, Pich V, Hofmann SG, Barlow DH. 2006. Tinnitus among Cambodian refugees: relationship to PTSD severity. J Trauma Stress 19: 541-546.
23. Horn AK, Eberhorn A, Hartig W, Ardeleanu P, Messoudi A, Buttner-Ennever JA. 2008. Perioculomotor cell groups in monkey and man defined by their histochemical and functional properties: reappraisal of the Edinger-Westphal nucleus. J Comp Neurol 507: 1317-1335.
24. Horn AK, Schulze C, Radtke-Schuller S. 2009. The Edinger-Westphal nucleus represents different functional cell groups in different species. Ann N Y Acad Sci 1164: 45-50.
25. Jenkins SA, Simmons DD. 2006. GABAergic neurons in the lateral superior olive of the hamster are distinguished by differential expression of GAD isoforms during development. Brain Res 1111: 12-25.
26. Kandler K, Kullmann PH, Ene FA, Kim G. 2002. Excitatory action of an immature glycinergic/GABAergic sound localization pathway. Physiol Behav 77: 583-587.
27. Kandler K, Clause A, Noh J. 2009. Tonotopic reorganization of developing auditory brainstem circuits. Nat Neurosci 12: 711-717.
28. Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, de Caprona D, Fritzsch B. 2001. Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429: 615-630.
29. Kaufman DL, Houser CR, Tobin AJ. 1991. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neurochem 56: 720-723.
30. Korada S, Schwartz IR. 1999. Development of GABA, glycine, and their receptors in the auditory brainstem of gerbil: a light and electron microscopic study. J Comp Neurol 409: 664-681.
31. Larsen E, Liberman MC. 2010. Contralateral cochlear effects of ipsilateral damage: no evidence for interaural coupling. Hear Res 260: 70-80.
32. Layton MG, Robertson D, Everett AW, Mulders WH, Yates GK. 2005. Cellular localization of voltage-gated calcium channels and synaptic vesicle-associated proteins in the guinea pig cochlea. J Mol Neurosci 27: 225-244.
33. Maley BE, Frick ML, Levey AI, Wainer BH, Elde RP. 1988. Immunohistochemistry of choline acetyltransferase in the guinea pig brain. Neurosci Lett 84: 137-142.
34. Matute C, Streit P. 1986. Monoclonal antibodies demonstrating GABA-like immunoreactivity. Histochemistry 86: 147-157.
35. Mazurek B, Stover T, Haupt H, Klapp BF, Adli M, Gross J, Szczepek AJ. 2009. Die Bedeutung von Stress: Seine Rolle im auditorischen System und bei der Tinnitusentstehung [The significance of stress: its role in the auditory system and the pathogenesis of tinnitus.]. HNO 1-11.
36. Mazurek B, Haupt H, Joachim R, Klapp BF, Stover T, Szczepek AJ. 2010. Stress induces transient auditory hypersensitivity in rats. Hear Res 259: 55-63.
37. Motts SD, Slusarczyk AS, Sowick CS, Schofield BR. 2008. Distribution of cholinergic cells in guinea pig brainstem. Neuroscience 154: 186-195.
38. Müller M. 1996. The cochlear place-frequency map of the adult and developing Mongolian gerbil. Hear Res 94: 148-156.
39. Nealen PM. 2005. An interspecific comparison using immunofluorescence reveals that synapse density in the avian song system is related to sex but not to male song repertoire size. Brain Res 1032: 50-62.
40. Pan W, Kastin AJ. 2008. Urocortin and the brain. Prog Neurobiol 84: 148-156.
41. Raji-Kubba J, Micevych PE, Simmons DD. 2002. The superior olivary complex of the hamster has multiple periods of cholinergic neuron development. J Chem Neuroanat 24: 75-93.
42. Raphael Y, Altschuler RA. 2003. Structure and innervation of the cochlea. Brain Res Bull 60: 397-422.
43. Rautenberg PL, Grothe B, Felmy F. 2009. Quantification of the three-dimensional morphology of coincidence detector neurons in the medial superior olive of gerbils during late postnatal development. J Comp Neurol 517: 385-396.
44. Reul JM, Holsboer F. 2002. Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Curr Opin Pharmacol 2: 23-33.
45. 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: 356-367.
46. Sanes DH, Merickel M, Rubel EW. 1989. Evidence for an alteration of the tonotopic map in the gerbil cochlea during development. J Comp Neurol 279: 436-444.
47. Simmons DD. 2002. Development of the inner ear efferent system across vertebrate species. J Neurobiol 53: 228-250.
48. Soghomonian JJ, Martin DL. 1998. Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci 19: 500-505.
49. Son YJ, Scranton TW, Sunderland WJ, Baek SJ, Miner JH, Sanes JR, Carlson SS. 2000. The synaptic vesicle protein SV2 is complexed with an alpha5-containing laminin on the nerve terminal surface. J Biol Chem 275: 451-460.
50. Suga N, Gao E, Zhang Y, Ma X, Olsen JF. 2000. The corticofugal system for hearing: recent progress. Proc Natl Acad Sci U S A 97: 11807-11814.
51. Tahera Y, Meltser I, Johansson P, Salman H, Canlon B. 2007. Sound conditioning protects hearing by activating the hypothalamic-pituitary-adrenal axis. Neurobiol Dis 25: 189-197.
52. Vasconcelos LA, Donaldson C, Sita LV, Casatti CA, Lotfi CF, Wang L, Cadinouche MZ, Frigo L, Elias CF, Lovejoy DA, Bittencourt JC. 2003. Urocortin in the central nervous system of a primate (Cebus apella): sequencing, immunohistochemical, and hybridization histochemical characterization. J Comp Neurol 463: 157-175.
53. Vaughan J, Donaldson C, Bittencourt J, Perrin MH, Lewis K, Sutton S, Chan R, Turnbull AV, Lovejoy D, Rivier C. 1995. Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor. Nature 378: 287-292.
54. Vetter DE, Adams JC, Mugnaini E. 1991. Chemically distinct rat olivocochlear neurons. Synapse (New York) 7: 21-43.
55. Vetter DE, Li C, Zhao L, Contarino A, Liberman MC, Smith GW, Marchuk Y, Koob GF, Heinemann SF, Vale W, Lee KF. 2002. Urocortin-deficient mice show hearing impairment and increased anxiety-like behavior. Nat Genet 31: 363-369.
56. Wang X, Su H, Copenhagen LD, Vaishnav S, Pieri F, Shope CD, Brownell WE, De Biasi M, Paylor R, Bradley A. 2002. Urocortin-deficient mice display normal stress-induced anxiety behavior and autonomic control but an impaired acoustic startle response. Mol Cell Biol 22: 6605-6610.
57. Warr WB. 1975. Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J Comp Neurol 161: 159-181.
58. Warr WB. 1992. Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR, editors. The mammalian auditory pathway: neuroanatomy. New York: Springer. p 410-48.
59. Warr WB, Guinan JJ Jr. 1979. Efferent innervation of the organ of corti: two separate systems. Brain Res 173: 152-155.
60. Warr WB, Guinan JJ Jr, White JS. 1986. Organization of the efferent fibers: The lateral and medial olivocochlear systems. In: Altschuler RA, Hoffman DW, Bobbin RP, editors. Neurobiology of hearing: the cochlea. New York: Raven Press. p 333-48.
61. Warr WB, Beck Boche JE, Neely ST. 1997. Efferent innervation of the inner hair cell region: origins and terminations of two lateral olivocochlear systems. Hear Res 108: 89-111.
62. Winer JA. 2005. Decoding the auditory corticofugal systems. Hear Res 207: 1-9.
63. Woolf NK, Ryan AF. 1984. The development of auditory function in the cochlea of the mongolian gerbil. Hear Res 13: 277-83.
64. Yapa WB. 1994. Social behaviour of the Mongolian gerbil Meriones unguiculatus, with special reference to acoustic communication [dissertation]. Ludwig-Maximilians-Universitaet Muenchen.
65. Zar JH. 1984. Biostatistical analysis, 2nd ed. Englewood Cliffs, NJ: Prentice-Hall.