Advertisement

Circadian Influences on the Auditory System

  • Christopher R. CederrothEmail author
  • Vasiliki Basinou
  • Jung-Sub Park
  • Barbara Canlon
Chapter

Abstract

In this chapter, we will deal with circadian rhythms and their influence on hearing and tinnitus. Circadian rhythms control bodily functions such as sleep, inflammation, metabolism, renal function, hormone secretion, as well as auditory functions. Animal studies have revealed that the auditory system has an inbuilt clock machinery that regulates sensitivity to noise throughout the day. Due to the detrimental consequences of disrupted circadian rhythms on human health (e.g., jet lag, shift workers), it is important to understand how the clock system regulates auditory function with the aim of providing new avenues for the development of targeted therapies.

References

  1. Abe M, Herzog ED, Yamazaki S, Straume M, Tei H, Sakaki Y, Menaker M, Block GD (2002) Circadian rhythms in isolated brain regions. J Neurosci 22:350–356PubMedGoogle Scholar
  2. Abraham U, Granada AE, Westermark PO, Heine M, Kramer A, Herzel H (2010) Coupling governs entrainment range of circadian clocks. Mol Syst Biol 6:438CrossRefPubMedPubMedCentralGoogle Scholar
  3. Akhtar RA, Reddy AB, Maywood ES, Clayton JD, King VM, Smith AG, Gant TW, Hastings MH, Kyriacou CP (2002) Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr Biol 12:540–550CrossRefPubMedGoogle Scholar
  4. Albrecht U (2002) Invited review: regulation of mammalian circadian clock genes. J Appl Physiol 92:1348–1355CrossRefPubMedGoogle Scholar
  5. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U (2000) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344–2347CrossRefPubMedGoogle Scholar
  6. Bartlang MS, Neumann ID, Slattery DA, Uschold-Schmidt N, Kraus D, Helfrich-Forster C, Reber SO (2012) Time matters: pathological effects of repeated psychosocial stress during the active, but not inactive, phase of male mice. J Endocrinol 215:425–437CrossRefPubMedGoogle Scholar
  7. Bartlang MS, Savelyev SA, Johansson AS, Reber SO, Helfrich-Forster C, Lundkvist GB (2014) Repeated psychosocial stress at night, but not day, affects the central molecular clock. Chronobiol Int 31:996–1007CrossRefPubMedGoogle Scholar
  8. Basner M, Babisch W, Davis A, Brink M, Clark C, Janssen S, Stansfeld S (2014) Auditory and non-auditory effects of noise on health. Lancet 383:1325–1332CrossRefPubMedGoogle Scholar
  9. Basinou V, Park JS, Cederroth CR, Canlon B (2017) Circadian regulation of auditory function. Hear Res 347:47–55Google Scholar
  10. Basner M, Brink M, Bristow A, de Kluizenaar Y, Finegold L, Hong J, Janssen SA, Klaeboe R, Leroux T, Liebl A, Matsui T, Schwela D, Sliwinska-Kowalska M, Sorqvist P (2015) ICBEN review of research on the biological effects of noise 2011–2014. Noise Health 17:57–82CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bozek K, Relogio A, Kielbasa SM, Heine M, Dame C, Kramer A, Herzel H (2009) Regulation of clock-controlled genes in mammals. PLoS One 4:e4882CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bozek K, Rosahl AL, Gaub S, Lorenzen S, Herzel H (2010) Circadian transcription in liver. Bio Systems 102:61–69CrossRefPubMedGoogle Scholar
  13. Cacace AT, McClelland WA, Weiner J, McFarland DJ (1996) Individual differences and the reliability of 2F1-F2 distortion-product otoacoustic emissions: effects of time-of-day, stimulus variables, and gender. J Speech Hear Res 39:1138–1148CrossRefPubMedGoogle Scholar
  14. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, Zhou QY (2002) Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417:405–410CrossRefPubMedGoogle Scholar
  15. Davidson AJ, Menaker M (2003) Birds of a feather clock together—sometimes: social synchronization of circadian rhythms. Curr Opin Neurobiol 13:765–769CrossRefPubMedGoogle Scholar
  16. Dibner C, Schibler U (2015) Circadian timing of metabolism in animal models and humans. J Intern Med 277:513–527CrossRefPubMedGoogle Scholar
  17. Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517–549CrossRefPubMedGoogle Scholar
  18. Dzirasa K, Coque L, Sidor MM, Kumar S, Dancy EA, Takahashi JS, McClung CA, Nicolelis MA (2010) Lithium ameliorates nucleus accumbens phase-signaling dysfunction in a genetic mouse model of mania. J Neurosci 30:16314–16323CrossRefPubMedPubMedCentralGoogle Scholar
  19. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O’Neill JS, Reddy AB (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–464PubMedPubMedCentralGoogle Scholar
  20. Elgoyhen AB, Langguth B, De Ridder D, Vanneste S (2015) Tinnitus: perspectives from human neuroimaging. Nat Rev Neurosci 16:632–642CrossRefPubMedGoogle Scholar
  21. Evans JA, Davidson AJ (2013) Health consequences of circadian disruption in humans and animal models. Prog Mol Biol Transl Sci 119:283–323CrossRefPubMedGoogle Scholar
  22. Faingold CL, Naritoku DK, Copley CA, Randall ME, Riaz A, Anderson CA, Arneric SP (1992) Glutamate in the inferior colliculus plays a critical role in audiogenic seizure initiation. Epilepsy Res 13:95–105CrossRefPubMedGoogle Scholar
  23. Fritzsch B, Tessarollo L, Coppola E, Reichardt LF (2004) Neurotrophins in the ear: their roles in sensory neuron survival and fiber guidance. Prog Brain Res 146:265–278CrossRefPubMedGoogle Scholar
  24. Gachon F, Fonjallaz P, Damiola F, Gos P, Kodama T, Zakany J, Duboule D, Petit B, Tafti M, Schibler U (2004a) The loss of circadian PAR bZip transcription factors results in epilepsy. Genes Dev 18:1397–1412CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gachon F, Nagoshi E, Brown SA, Ripperger J, Schibler U (2004b) The mammalian circadian timing system: from gene expression to physiology. Chromosoma 113:103–112CrossRefPubMedGoogle Scholar
  26. Gachon F, Olela FF, Schaad O, Descombes P, Schibler U (2006) The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab 4:25–36CrossRefPubMedGoogle Scholar
  27. Germain A, Kupfer DJ (2008) Circadian rhythm disturbances in depression. Hum Psychopharmacol 23:571–585CrossRefPubMedPubMedCentralGoogle Scholar
  28. Guilding C, Piggins HD (2007) Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25:3195–3216CrossRefPubMedGoogle Scholar
  29. Guler AD, Ecker JL, Lall GS, Haq S, Altimus CM, Liao HW, Barnard AR, Cahill H, Badea TC, Zhao H, Hankins MW, Berson DM, Lucas RJ, Yau KW, Hattar S (2008) Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453:102–105CrossRefPubMedPubMedCentralGoogle Scholar
  30. Haggerty HS, Lusted HS, Morton SC (1993) Statistical quantification of 24-hour and monthly variabilities of spontaneous otoacoustic emission frequency in humans. Hear Res 70:31–49CrossRefPubMedGoogle Scholar
  31. Halberg F, Jacobsen E, Wadsworth G, Bittner JJ (1958) Audiogenic abnormality spectra, twenty-four hour periodicity, and lighting. Science 128:657–658CrossRefPubMedGoogle Scholar
  32. Hannibal J, Fahrenkrug J (2002) Melanopsin: a novel photopigment involved in the photoentrainment of the brain’s biological clock? Ann Med 34:401–407CrossRefPubMedGoogle Scholar
  33. Hattar S, Liao HW, Takao M, Berson DM, Yau KW (2002) Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295:1065–1070CrossRefPubMedPubMedCentralGoogle Scholar
  34. Haynes P (2015) Application of cognitive behavioral therapies for comorbid insomnia and depression. Sleep Med Clin 10:77–84CrossRefPubMedGoogle Scholar
  35. Haynes PL, Gengler D, Kelly M (2016a) Social rhythm therapies for mood disorders: an update. Curr Psychiatry Rep 18:75CrossRefPubMedPubMedCentralGoogle Scholar
  36. Haynes PL, Kelly M, Warner L, Quan SF, Krakow B, Bootzin RR (2016b) Cognitive behavioral social rhythm group therapy for veterans with posttraumatic stress disorder, depression, and sleep disturbance: results from an open trial. J Affect Disord 192:234–243CrossRefPubMedGoogle Scholar
  37. van der Horst GT, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, de Wit J, Verkerk A, Eker AP, van Leenen D, Buijs R, Bootsma D, Hoeijmakers JH, Yasui A (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398:627–630CrossRefPubMedGoogle Scholar
  38. Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB (2009) Harmonics of circadian gene transcription in mammals. PLoS Genet 5:e1000442CrossRefPubMedPubMedCentralGoogle Scholar
  39. Ishida A, Mutoh T, Ueyama T, Bando H, Masubuchi S, Nakahara D, Tsujimoto G, Okamura H (2005) Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab 2:297–307CrossRefPubMedGoogle Scholar
  40. Jang SW, Liu X, Yepes M, Shepherd KR, Miller GW, Liu Y, Wilson WD, Xiao G, Blanchi B, Sun YE, Ye K (2010) A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc Natl Acad Sci USA 107:2687–2692CrossRefPubMedPubMedCentralGoogle Scholar
  41. Jiang WG, Li SX, Zhou SJ, Sun Y, Shi J, Lu L (2011) Chronic unpredictable stress induces a reversible change of PER2 rhythm in the suprachiasmatic nucleus. Brain Res 1399:25–32CrossRefPubMedGoogle Scholar
  42. Kalsbeek A, La Fleur S, Van Heijningen C, Buijs RM (2004) Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J Neurosci 24:7604–7613CrossRefPubMedGoogle Scholar
  43. Kiessling S, Eichele G, Oster H (2010) Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. J Clin Invest 120:2600–2609CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, Antoch MP (2006) Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev 20:1868–1873CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kondratov RV, Gorbacheva VY, Antoch MP (2007) The role of mammalian circadian proteins in normal physiology and genotoxic stress responses. In: Gerald PS (ed) Current topics in developmental biology, vol 78. Academic Press, Cambridge, MA, pp 173–216Google Scholar
  46. Korencic A, Kosir R, Bordyugov G, Lehmann R, Rozman D, Herzel H (2014) Timing of circadian genes in mammalian tissues. Sci Rep 4:5782CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lamia KA, Storch KF, Weitz CJ (2008) Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci USA 105:15172–15177CrossRefPubMedPubMedCentralGoogle Scholar
  48. Lamia KA, Papp SJ, Yu RT, Barish GD, Uhlenhaut NH, Jonker JW, Downes M, Evans RM (2011) Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 480:552–556PubMedPubMedCentralGoogle Scholar
  49. Le Martelot G, Claudel T, Gatfield D, Schaad O, Kornmann B, Lo Sasso G, Moschetta A, Schibler U (2009) REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol 7:e1000181CrossRefPubMedPubMedCentralGoogle Scholar
  50. Loh DH, Dragich JM, Kudo T, Schroeder AM, Nakamura TJ, Waschek JA, Block GD, Colwell CS (2011) Effects of vasoactive intestinal peptide genotype on circadian gene expression in the suprachiasmatic nucleus and peripheral organs. J Biol Rhythm 26:200–209CrossRefGoogle Scholar
  51. Lowrey PL, Takahashi JS (2004) Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet 5:407–441CrossRefPubMedPubMedCentralGoogle Scholar
  52. Malek ZS, Sage D, Pevet P, Raison S (2007) Daily rhythm of tryptophan hydroxylase-2 messenger ribonucleic acid within raphe neurons is induced by corticoid daily surge and modulated by enhanced locomotor activity. Endocrinology 148:5165–5172CrossRefPubMedGoogle Scholar
  53. Marcheva B, Ramsey KM, Buhr ED, Kobayashi Y, Su H, Ko CH, Ivanova G, Omura C, Mo S, Vitaterna MH, Lopez JP, Philipson LH, Bradfield CA, Crosby SD, JeBailey L, Wang X, Takahashi JS, Bass J (2010) Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 466:627–631CrossRefPubMedPubMedCentralGoogle Scholar
  54. Mauvoisin D, Dayon L, Gachon F, Kussmann M (2015) Proteomics and circadian rhythms: it’s all about signaling! Proteomics 15:310–317CrossRefPubMedGoogle Scholar
  55. McClung CA, Sidiropoulou K, Vitaterna M, Takahashi JS, White FJ, Cooper DC, Nestler EJ (2005) Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc Natl Acad Sci USA 102:9377–9381CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mehra A, Baker CL, Loros JJ, Dunlap JC (2009) Post-translational modifications in circadian rhythms. Trends Biochem Sci 34:483–490CrossRefPubMedPubMedCentralGoogle Scholar
  57. Meltser I, Canlon B (2011) Protecting the auditory system with glucocorticoids. Hear Res 281:47–55CrossRefPubMedGoogle Scholar
  58. Meltser I, Cederroth CR, Basinou V, Savelyev S, Lundkvist GS, Canlon B (2014) TrkB-mediated protection against circadian sensitivity to noise trauma in the murine cochlea. Curr Biol 24:658–663CrossRefPubMedPubMedCentralGoogle Scholar
  59. Menaker M, Eskin A (1966) Entrainment of circadian rhythms by sound in Passer domesticus. Science 154:1579–1581CrossRefPubMedGoogle Scholar
  60. Mohawk JA, Green CB, Takahashi JS (2012) Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35:445–462CrossRefPubMedPubMedCentralGoogle Scholar
  61. Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201–206CrossRefPubMedGoogle Scholar
  62. Moss TG, Carney CE, Haynes P, Harris AL (2015) Is daily routine important for sleep? An investigation of social rhythms in a clinical insomnia population. Chronobiol Int 32:92–102CrossRefPubMedGoogle Scholar
  63. O’Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F, Bouget FY, Reddy AB, Millar AJ (2011) Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–558CrossRefPubMedPubMedCentralGoogle Scholar
  64. Oishi K, Amagai N, Shirai H, Kadota K, Ohkura N, Ishida N (2005) Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver. DNA Res 12:191–202CrossRefPubMedGoogle Scholar
  65. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320CrossRefPubMedGoogle Scholar
  66. Paranjpe DA, Sharma VK (2005) Evolution of temporal order in living organisms. J Circadian Rhythms 3:7CrossRefPubMedPubMedCentralGoogle Scholar
  67. Park JS, Cederroth CR, Basinou V, Lundkvist GS, Meltser I, Canlon B (2016) Identification of a circadian clock in the inferior colliculus and its dysregulation by noise exposure. J Neurosci 36(20):5509–5519CrossRefPubMedPubMedCentralGoogle Scholar
  68. Perelis M, Marcheva B, Ramsey KM, Schipma MJ, Hutchison AL, Taguchi A, Peek CB, Hong H, Huang W, Omura C, Allred AL, Bradfield CA, Dinner AR, Barish GD, Bass J (2015) Pancreatic beta cell enhancers regulate rhythmic transcription of genes controlling insulin secretion. Science 350:aac4250CrossRefPubMedPubMedCentralGoogle Scholar
  69. Ralph MR, Foster RG, Davis FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–978CrossRefPubMedGoogle Scholar
  70. Reddy AB, Maywood ES, Karp NA, King VM, Inoue Y, Gonzalez FJ, Lilley KS, Kyriacou CP, Hastings MH (2007) Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology 45:1478–1488CrossRefPubMedGoogle Scholar
  71. Reebs SG (1989) Acoustical entrainment of circadian activity rhythms in house sparrows: constant light is not necessary. Ethology 80:172–181CrossRefGoogle Scholar
  72. Reinke H, Saini C, Fleury-Olela F, Dibner C, Benjamin IJ, Schibler U (2008) Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor. Genes Dev 22:331–345CrossRefPubMedPubMedCentralGoogle Scholar
  73. Richards J, Gumz ML (2012) Advances in understanding the peripheral circadian clocks. FASEB J 26:3602–3613CrossRefPubMedPubMedCentralGoogle Scholar
  74. Roybal K, Theobold D, Graham A, DiNieri JA, Russo SJ, Krishnan V, Chakravarty S, Peevey J, Oehrlein N, Birnbaum S, Vitaterna MH, Orsulak P, Takahashi JS, Nestler EJ, Carlezon WA Jr, McClung CA (2007) Mania-like behavior induced by disruption of CLOCK. Proc Natl Acad Sci USA 104:6406–6411CrossRefPubMedPubMedCentralGoogle Scholar
  75. Ruttiger L, Singer W, Panford-Walsh R, Matsumoto M, Lee SC, Zuccotti A, Zimmermann U, Jaumann M, Rohbock K, Xiong H, Knipper M (2013) The reduced cochlear output and the failure to adapt the central auditory response causes tinnitus in noise exposed rats. PLoS One 8:e57247CrossRefPubMedPubMedCentralGoogle Scholar
  76. Schaette R, McAlpine D (2011) Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J Neurosci 31:13452–13457CrossRefPubMedGoogle Scholar
  77. Spencer S, Torres-Altoro MI, Falcon E, Arey R, Marvin M, Goldberg M, Bibb JA, McClung CA (2012) A mutation in CLOCK leads to altered dopamine receptor function. J Neurochem 123:124–134CrossRefPubMedPubMedCentralGoogle Scholar
  78. Spencer S, Falcon E, Kumar J, Krishnan V, Mukherjee S, Birnbaum SG, McClung CA (2013) Circadian genes Period 1 and Period 2 in the nucleus accumbens regulate anxiety-related behavior. Eur J Neurosci 37:242–250CrossRefPubMedGoogle Scholar
  79. Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69(6):1583CrossRefPubMedPubMedCentralGoogle Scholar
  80. Storch K-F, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83CrossRefPubMedGoogle Scholar
  81. Tahera Y, Meltser I, Johansson P, Canlon B (2006) Restraint stress modulates glucocorticoid receptors and nuclear factor kappa B in the cochlea. Neuroreport 17:879–882CrossRefPubMedGoogle Scholar
  82. Ueda HR, Chen W, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, Iino M, Shigeyoshi Y, Hashimoto S (2002) A transcription factor response element for gene expression during circadian night. Nature 418:534–539CrossRefPubMedGoogle Scholar
  83. Vikhe Patil K, Canlon B, Cederroth CR (2015) High quality RNA extraction of the mammalian cochlea for qRT-PCR and transcriptome analyses. Hear Res 325:42–48CrossRefPubMedGoogle Scholar
  84. Waite EJ, McKenna M, Kershaw Y, Walker JJ, Cho K, Piggins HD, Lightman SL (2012) Ultradian corticosterone secretion is maintained in the absence of circadian cues. Eur J Neurosci 36:3142–3150CrossRefPubMedGoogle Scholar
  85. Wan G, Gomez-Casati ME, Gigliello AR, Liberman MC, Corfas G (2014) Neurotrophin-3 regulates ribbon synapse density in the cochlea and induces synapse regeneration after acoustic trauma. Elife 3:e03564CrossRefPubMedCentralGoogle Scholar
  86. Yamamoto T, Nakahata Y, Soma H, Akashi M, Mamine T, Takumi T (2004) Transcriptional oscillation of canonical clock genes in mouse peripheral tissues. BMC Mol Biol 5:18CrossRefPubMedPubMedCentralGoogle Scholar
  87. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682–685CrossRefPubMedGoogle Scholar
  88. Yamazaki S, Yoshikawa T, Biscoe EW, Numano R, Gallaspy LM, Soulsby S, Papadimas E, Pezuk P, Doyle SE, Tei H, Sakaki Y, Block GD, Menaker M (2009) Ontogeny of circadian organization in the rat. J Biol Rhythm 24:55–63CrossRefGoogle Scholar
  89. Yonovitz A, Fisch JE (1991) Circadian rhythm dependent kanamycin-induced hearing loss in rodents assessed by auditory brainstem responses. Acta Otolaryngol 111:1006–1012PubMedGoogle Scholar
  90. Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, Menaker M, Takahashi JS (2004) PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 101:5339–5346CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zheng B, Albrecht U, Kaasik K, Sage M, Lu W, Vaishnav S, Li Q, Sun ZS, Eichele G, Bradley A, Lee CC (2001) Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell 105:683–694CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Christopher R. Cederroth
    • 1
    Email author
  • Vasiliki Basinou
    • 1
  • Jung-Sub Park
    • 1
  • Barbara Canlon
    • 1
  1. 1.Experimental Audiology Group, Department of Physiology and PharmacologyKarolinska InstitutetStockholmSweden

Personalised recommendations