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Apoptotic mechanisms after repeated noise trauma in the mouse medial geniculate body and primary auditory cortex

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Abstract

A correlation between noise-induced apoptosis and cell loss has previously been shown after a single noise exposure in the cochlear nucleus, inferior colliculus, medial geniculate body (MGB) and primary auditory cortex (AI). However, repeated noise exposure is the most common situation in humans and a major risk factor for the induction of noise-induced hearing loss (NIHL). The present investigation measured cell death pathways using terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) in the dorsal, medial and ventral MGB (dMGB, mMGB and vMGB) and six layers of the AI (AI-1 to AI-6) in mice (NMRI strain) after a second noise exposure (double-exposure group). Therefore, a single noise exposure group has been investigated 7 (7-day-group-single) or 14 days (14-day-group-single) after noise exposure (3 h, 5–20 kHz, 115 dB SPL peak-to-peak). The double-exposure group received the same noise trauma for a second time 7 days after the initial exposure and was either TUNEL-stained immediately (7-day-group-double) or 1 week later (14-day-group-double) and data were compared to the corresponding single-trauma group as well as to an unexposed control group. It was shown that TUNEL increased immediately after the second noise exposure in AI-3 and stayed upregulated in the 14-day-group-double. A significant increase in TUNEL was also seen in the 14-day-group-double in vMGB, mMGB and AI-1. The present results show for the first time the influence of a repeated noise trauma on cell death mechanisms in thalamic and cortical structures and might contribute to the understanding of pathophysiological findings and psychoacoustic phenomena accompanying NIHL.

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References

  • Aarnisalo AA, Pirvola U, Liang XQ, Miller J, Ylikoski J (2000) Apoptosis in auditory brainstem neurons after a severe noise trauma of the organ of Corti: intracochlear GDNF treatment reduces the number of apoptotic cells. ORL J Otorhinolaryngol Relat Spec 62:330–334

    Article  CAS  PubMed  Google Scholar 

  • Ahroon WA, Hamernik RP (2000) The effects of interrupted noise exposures on the noise-damaged cochlea. Hear Res 143:103–109

    Article  CAS  PubMed  Google Scholar 

  • Alvarado JC, Fuentes-Santamaria V, Gabaldon-Ull MC, Jareno-Flores T, Miller JM, Juiz JM (2016) Noise-induced “toughening” effect in Wistar rats: enhanced auditory brainstem responses are related to calretinin and nitric oxide synthase upregulation. Front Neuroanat 10:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Basta D, Tzschentke B, Ernst A (2005) Noise-induced cell death in the mouse medial geniculate body and primary auditory cortex. Neurosci Lett 381:199–204

    Article  CAS  PubMed  Google Scholar 

  • Bose M et al (2010) Effect of the environment on the dendritic morphology of the rat auditory cortex. Synapse 64:97–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calford MB (1983) The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350–2364

    CAS  PubMed  Google Scholar 

  • Calford MB, Aitkin LM (1983) Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3:2365–2380

    CAS  PubMed  Google Scholar 

  • Caspary DM, Llano DA (2017) Auditory thalamic circuits and GABAA receptor function: putative mechanisms in tinnitus pathology. Hear Res 349:197–207

    Article  CAS  PubMed  Google Scholar 

  • Choi DW (1995) Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci 18:58–60

    Article  CAS  PubMed  Google Scholar 

  • Coomber B, Berger JI, Kowalkowski VL, Shackleton TM, Palmer AR, Wallace MN (2014) Neural changes accompanying tinnitus following unilateral acoustic trauma in the guinea pig. Eur J Neurosci 40:2427–2441

    Article  PubMed  PubMed Central  Google Scholar 

  • Coordes A, Groschel M, Ernst A, Basta D (2012) Apoptotic cascades in the central auditory pathway after noise exposure. J Neurotrauma 29:1249–1254

    Article  PubMed  Google Scholar 

  • Eggermont JJ (2017) Effects of long-term non-traumatic noise exposure on the adult central auditory system. Hearing problems without hearing loss. Hear Res 352:12–22

    Article  PubMed  Google Scholar 

  • Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27:676–682

    Article  CAS  PubMed  Google Scholar 

  • Ehret GR, Romand R (1997) The central auditory system. Oxford University Press, Oxford

    Google Scholar 

  • Eimerl S, Schramm M (1994) The quantity of calcium that appears to induce neuronal death. J Neurochem 62:1223–1226

    Article  CAS  PubMed  Google Scholar 

  • Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493–501

    Article  CAS  PubMed  Google Scholar 

  • Godfrey DA, Kaltenbach JA, Chen K, Ilyas O (2013) Choline acetyltransferase activity in the hamster central auditory system and long-term effects of intense tone exposure. J Neurosci Res 91:987–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Hermann R (1995) In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 21:1465–1468

    CAS  PubMed  Google Scholar 

  • Gröschel M, Götze R, Ernst A, Basta D (2010) Differential impact of temporary and permanent noise-induced hearing loss on neuronal cell density in the mouse central auditory pathway. J Neurotrauma 27:1499–1507

    Article  PubMed  Google Scholar 

  • Gröschel M, Müller S, Götze R, Ernst A, Basta D (2011) The possible impact of noise-induced Ca2+ -dependent activity in the central auditory pathway: a manganese-enhanced MRI study. Neuroimage 57:190–197

    Article  PubMed  Google Scholar 

  • Hackett TA (2011) Information flow in the auditory cortical network. Hear Res 271:133–146

    Article  PubMed  Google Scholar 

  • Hackett TA (2015) Anatomic organization of the auditory cortex. In: Michael J, Aminoff FB, Dick FS (eds) Handbook of clinical neurology, vol 129, 6th edn. Elsevier, Amsterdam, pp 27–53

    Google Scholar 

  • Hu BH, Henderson D, Nicotera TM (2002) Involvement of apoptosis in progression of cochlear lesion following exposure to intense noise. Hear Res 166:62–71

    Article  PubMed  Google Scholar 

  • Hu BH, Henderson D, Nicotera TM (2006) Extremely rapid induction of outer hair cell apoptosis in the chinchilla cochlea following exposure to impulse noise. Hear Res 211:16–25

    Article  PubMed  Google Scholar 

  • Huang T et al (2000) Oxidative stress-induced apoptosis of cochlear sensory cells: otoprotective strategies. Int J Dev Neurosci 18:259–270

    Article  CAS  PubMed  Google Scholar 

  • Ito T, Bishop DC, Oliver DL (2016) Functional organization of the local circuit in the inferior colliculus. Anat Sci Int 91:22–34

    Article  Google Scholar 

  • Jacono AA, Hu B, Kopke RD, Henderson D, Van De Water TR, Steinman HM (1998) Changes in cochlear antioxidant enzyme activity after sound conditioning and noise exposure in the chinchilla. Hear Res 117:31–38

    Article  CAS  PubMed  Google Scholar 

  • Johnson EM Jr, Koike T, Franklin J (1992) A “calcium set-point hypothesis” of neuronal dependence on neurotrophic factor. Exp Neurol 115:163–166

    Article  PubMed  Google Scholar 

  • Kaltenbach JA, McCaslin DL (1996) Increases in spontaneous activity in the dorsal cochlear nucleus following exposure to high intensity sound: a possible neural correlate of tinnitus. Aud Neurosci 3:57–78

    PubMed  PubMed Central  Google Scholar 

  • Kane EC (1974) Patterns of degeneration in the caudal cochlear nucleus of the cat after cochlear ablation. Anat Rec 179:67–91

    Article  CAS  PubMed  Google Scholar 

  • Kelly JP, Wong D (1981) Laminar connections of the cat’s auditory cortex. Brain Res 212:1–15

    Article  CAS  PubMed  Google Scholar 

  • Kiefer L, Schauen A, Abendroth S, Gaese BH, Nowotny M (2015) Variation in acoustic overstimulation changes tinnitus characteristics. Neuroscience 310:176–187

    Article  CAS  PubMed  Google Scholar 

  • Kroemer G et al (2009) Classification of cell death: recommendations of the nomenclature committee on cell death 2009. Cell Death Differ 16:3–11

    Article  CAS  PubMed  Google Scholar 

  • Lee AC, Godfrey DA (2014) Cochlear damage affects neurotransmitter chemistry in the central auditory system. Front Neurol 5:227

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee CC, Sherman SM (2010) Topography and physiology of ascending streams in the auditory tectothalamic pathway. Proc Natl Acad Sci USA 107:372–377

    Article  CAS  PubMed  Google Scholar 

  • Lee CC, Winer JA (2008) Connections of cat auditory cortex: I. Thalamocortical system. J Comp Neurol 507:1879–1900

    Article  PubMed  PubMed Central  Google Scholar 

  • Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146:3–15

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mandairon N, Jourdan F, Didier A (2003) Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 119:507–516

    Article  CAS  PubMed  Google Scholar 

  • Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793–807

    Article  CAS  PubMed  Google Scholar 

  • 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 24:658–663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michiels C (2004) Physiological and pathological responses to hypoxia. Am J Pathol 164:1875–1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitani A, Shimokouchi M (1985) Neuronal connections in the primary auditory cortex: an electrophysiological study in the cat. J Comp Neurol 235:417–429

    Article  CAS  PubMed  Google Scholar 

  • Mitani A, Itoh K, Nomura S, Kudo M, Kaneko T, Mizuno N (1984) Thalamocortical projections to layer I of the primary auditory cortex in the cat: a horseradish peroxidase study. Brain Res 310:347–350

    Article  CAS  PubMed  Google Scholar 

  • Møller AR (2000) Hearing—anatomy, physiology and disorders of the auditory system, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  • Morest DK (1964) The neuronal architecture of the medial geniculate body of the cat. J Anat 98:611–630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Negoescu A et al (1996) In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparations. J Histochem Cytochem 44:959–968

    Article  CAS  PubMed  Google Scholar 

  • Negoescu A, Guillermet C, Lorimier P, Brambilla E, Labat-Moleur F (1998) Importance of DNA fragmentation in apoptosis with regard to TUNEL specificity. Biomed Pharmacother 52:252–258

    Article  CAS  PubMed  Google Scholar 

  • Niimi K, Naito F (1974) Cortical projections of the medial geniculate body in the cat. Exp Brain Res 19:326–342

    Article  CAS  PubMed  Google Scholar 

  • Norena AJ, Eggermont JJ (2003) Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res 183:137–153

    Article  CAS  PubMed  Google Scholar 

  • Nys J, Scheyltjens I, Arckens L (2015) Visual system plasticity in mammals: the story of monocular enucleation-induced vision loss. Front Syst Neurosci 9:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Ologe FE, Olajide TG, Nwawolo CC, Oyejola BA (2008) Deterioration of noise-induced hearing loss among bottling factory workers. J Laryngol Otol 122:786–794

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, London

    Google Scholar 

  • Pickles JO (2015) Auditory pathways: anatomy and physiology. In: Michael J, Aminoff FB, Dick FS (eds) Handbook of clinical neurology, vol 129, 1st edn. Elsevier, Amsterdam, pp 3–25

    Google Scholar 

  • Rajan R (1998) Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci 1:138–143

    Article  CAS  PubMed  Google Scholar 

  • Ryan AF, Axelsson GA, Woolf NK (1992) Central auditory metabolic activity induced by intense noise exposure. Hear Res 61:24–30

    Article  CAS  PubMed  Google Scholar 

  • Säljö A, Bao F, Jingshan S, Hamberger A, Hansson HA, Haglid KG (2002) Exposure to short-lasting impulse noise causes neuronal c-Jun expression and induction of apoptosis in the adult rat brain. J Neurotrauma 19:985–991

    Article  PubMed  Google Scholar 

  • Salvi RJ, Wang J, Ding D (2000) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147:261–274

    Article  CAS  PubMed  Google Scholar 

  • Sattler R, Tymianski M (2001) Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 24:107–129

    Article  CAS  PubMed  Google Scholar 

  • Sekiya T et al (2009) Selective vulnerability of adult cochlear nucleus neurons to de-afferentation by mechanical compression. Exp Neurol 218:117–123

    Article  PubMed  Google Scholar 

  • Sekiya T, Viberg A, Kojima K, Sakamoto T, Nakagawa T, Ito J, Canlon B (2012) Trauma-specific insults to the cochlear nucleus in the rat. J Neurosci Res 90:1924–1931

    Article  CAS  PubMed  Google Scholar 

  • WHO (2015) World Health Organization Department for Management of nuncommunicable diseases—1.1 billion people at risk of hearing loss. http://www.who.int/mediacentre/news/releases/2015/ear-care/en/. Accessed 12 Dec 2016

  • Winer JA, Saint Marie RL, Larue DT, Oliver DL (1996) GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. Proc Natl Acad Sci USA 93:8005–8010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You Y, Gupta VK, Graham SL, Klistorner A (2012) Anterograde degeneration along the visual pathway after optic nerve injury. PLoS One 7:e52061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu SP, Canzoniero LM, Choi DW (2001) Ion homeostasis and apoptosis. Curr Opin Cell Biol 13:405–411

    Article  CAS  PubMed  Google Scholar 

  • Yu CH, Moon CT, Sur JH, Chun YI, Choi WH, Yhee JY (2011) Serial expression of hypoxia inducible factor-1alpha and neuronal apoptosis in hippocampus of rats with chronic ischemic brain. J Korean Neurosurg Soc 50:481–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Moritz Gröschel.

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The present work was supported by the Deutsche Forschungsgemeinschaft DFG (Grant number GR 3519/3-1).

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Fröhlich, F., Ernst, A., Strübing, I. et al. Apoptotic mechanisms after repeated noise trauma in the mouse medial geniculate body and primary auditory cortex. Exp Brain Res 235, 3673–3682 (2017). https://doi.org/10.1007/s00221-017-5091-4

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