Noise induced hearing loss impairs spatial learning/memory and hippocampal neurogenesis in mice

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Liu, Lijie ^a   Shen, Pei ^a   He, Tingting ^a   Chang, Ying ^a   Shi, Lijuan ^a   Tao, Shan ^a   Li, Xiaowei ^a   Xun, Qingying ^a   Guo, Xiaojing ^a,b   Yu, Zhiping ^c   Wang, Jian ^a,c  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL; BLOOD; CBA MOUSE; HIPPOCAMPUS; METABOLISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NOISE INJURY; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; SPATIAL LEARNING; SPATIAL MEMORY;

ANIMALS; CORTICOSTERONE; HEARING LOSS, NOISE-INDUCED; HIPPOCAMPUS; MICE; MICE, INBRED CBA; NEUROGENESIS; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SPATIAL LEARNING; SPATIAL MEMORY; SUPEROXIDE DISMUTASE;

EID: 84957564685     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20374     Document Type: Article

References (61)

1. Tucci, D., Merson, M. H. & Wilson, B. S. A summary of the literature on global hearing impairment: current status and priorities for action. Otol Neurotol 31, 31-41 (2010).
2. Agrawal, Y., Platz, E. A. & Niparko, J. K. Prevalence of hearing loss and differences by demographic characteristics among US adults: data from the National Health and Nutrition Examination Survey, 1999-2004. Arch Intern Med 168, 1522-1530, doi: 10.1001/archinte.168.14.1522 (2008).
3. Cruickshanks, K. J. et al. Prevalence of hearing loss in older adults in Beaver Dam, Wisconsin. The Epidemiology of Hearing Loss Study. Am J Epidemiol 148, 879-886 (1998).
4. Nelson, D. I., Nelson, R. Y., Concha-Barrientos, M. & Fingerhut, M. The global burden of occupational noise-induced hearing loss. American journal of industrial medicine 48, 446-458, doi: 10.1002/ajim.20223 (2005).
5. Basner, M. et al. Auditory and non-auditory effects of noise on health. Lancet 383, 1325-1332, doi: 10.1016/S0140-6736(13)61613-X (2014).
6. Cheng, L., Wang, S. H., Chen, Q. C. & Liao, X. M. Moderate noise induced cognition impairment of mice and its underlying mechanisms. Physiol Behav 104, 981-988, doi: 10.1016/j.physbeh.2011.06.018 (2011).
7. Cui, B., Wu, M. & She, X. Effects of chronic noise exposure on spatial learning and memory of rats in relation to neurotransmitters and NMDAR2B alteration in the hippocampus. Journal of occupational health 51, 152-158 (2009).
8. Jauregui-Huerta, F. et al. Chronic exposure of juvenile rats to environmental noise impairs hippocampal cell proliferation in adulthood. Noise Health 13, 286-291, doi:10.4103/1463-1741.82961 (2011).
9. Wright, B., Peters, E., Ettinger, U., Kuipers, E. & Kumari, V. Understanding noise stress-induced cognitive impairment in healthy adults and its implications for schizophrenia. Noise Health 16, 166-176, doi:10.4103/1463-1741.134917 (2014).
10. Helfer, T. M. et al. Noise-induced hearing injury and comorbidities among postdeployment U.S. Army soldiers: April 2003-June 2009. Am J Audiol 20, 33-41, doi: 10.1044/1059-0889(2011/10-0033) (2011).
11. Cave, K. M., Cornish, E. M. & Chandler, D. W. Blast injury of the ear: clinical update from the global war on terror. Military medicine 172, 726-730 (2007).
12. Belanger, H. G., Kretzmer, T., Yoash-Gantz, R., Pickett, T. & Tupler, L. A. Cognitive sequelae of blast-related versus other mechanisms of brain trauma. J Int Neuropsychol Soc 15, 1-8, doi: 10.1017/S1355617708090036 (2009).
13. Chengzhi, C. et al. Recovery of chronic noise exposure induced spatial learning and memory deficits in young male Sprague-Dawley rats. Journal of occupational health 53, 157-163 (2011).
14. Hirano, Y. et al. Effect of unpleasant loud noise on hippocampal activities during picture encoding: an fMRI study. Brain Cogn 61, 280-285, doi: 10.1016/j.bandc.2006.02.003 (2006).
15. Kraus, K. S. & Canlon, B. Neuronal connectivity and interactions between the auditory and limbic systems. Effects of noise and tinnitus. Hear Res 288, 34-46, doi: 10.1016/j.heares.2012.02.009 (2012).
16. Yu, Y. F., Zhai, F., Dai, C. F. & Hu, J. J. The relationship between age-related hearing loss and synaptic changes in the hippocampus of C57BL/6J mice. Exp Gerontol 46, 716-722, doi: 10.1016/j.exger.2011.04.007 (2011).
17. Kraus, K. S. et al. Noise trauma impairs neurogenesis in the rat hippocampus. Neuroscience 167, 1216-1226, doi: 10.1016/j.neuroscience.2010.02.071 S0306-4522(10)00305-2 (2010).
18. Cui, B., Wu, M., She, X. & Liu, H. Impulse noise exposure in rats causes cognitive deficits and changes in hippocampal neurotransmitter signaling and tau phosphorylation. Brain Res 1427, 35-43, doi: S0006-8993(11)01540-X10.1016/j.brainres.2011.08.035 (2011).
19. Xu, J., Yu, L., Cai, R., Zhang, J. & Sun, X. Early continuous white noise exposure alters auditory spatial sensitivity and expression of GAD65 and GABAA receptor subunits in rat auditory cortex. Cereb Cortex 20, 804-812, doi: 10.1093/cercor/bhp143 (2010).
20. Rabat, A., Bouyer, J. J., George, O., Le Moal, M. & Mayo, W. Chronic exposure of rats to noise: relationship between long-term memory deficits and slow wave sleep disturbances. Behav Brain Res 171, 303-312, doi: S0166-4328(06)00210-5 10.1016/j.bbr.2006.04.007 (2006).
21. Stansfeld, S. A. et al. Aircraft and road traffic noise and children's cognition and health: a cross-national study. Lancet 365, 1942-1949, doi: S0140-6736(05)66660-3 10.1016/S0140-6736(05)66660-3 (2005).
22. Haines, M. M., Stansfeld, S. A., Job, R. F., Berglund, B. & Head, J. Chronic aircraft noise exposure, stress responses, mental health and cognitive performance in school children. Psychol Med 31, 265-277 (2001).
23. Arnsten, A. F. & Goldman-Rakic, P. S. Noise stress impairs prefrontal cortical cognitive function in monkeys: evidence for a hyperdopaminergic mechanism. Arch Gen Psychiatry 55, 362-368 (1998).
24. Manikandan, S. et al. Effects of chronic noise stress on spatial memory of rats in relation to neuronal dendritic alteration and free radical-imbalance in hippocampus and medial prefrontal cortex. Neurosci Lett 399, 17-22, doi: 10.1016/j.neulet.2006.01.037 (2006).
25. Schoenfeld, T. J. & Gould, E. Stress, stress hormones, and adult neurogenesis. Exp Neurol 233, 12-21, doi: S0014-4886(11)00022-710.1016/j.expneurol.2011.01.008 (2012).
26. Li, W. Z. et al. Glucocorticoids increase impairments in learning and memory due to elevated amyloid precursor protein expression and neuronal apoptosis in 12-month old mice. Eur J Pharmacol 628, 108-115, doi: 10.1016/j.ejphar.2009.11.045 (2010).
27. Schoenfeld, T. J. & Gould, E. Differential effects of stress and glucocorticoids on adult neurogenesis. Curr Top Behav Neurosci 15, 139-164, doi:10.1007/7854-2012-233 (2013).
28. Wang, Q. et al. Glucocorticoid receptor protein expression in human hippocampus; stability with age. Neurobiol Aging 34, 1662-1673, doi: 10.1016/j.neurobiolaging.2012.11.019 (2013).
29. Lucassen, P. J. et al. Neuropathology of stress. Acta Neuropathol 127, 109-135, doi: 10.1007/s00401-013-1223-5 (2014).
30. Lucassen, P. J. et al. Regulation of Adult Neurogenesis and Plasticity by (Early) Stress, Glucocorticoids, and Inflammation. Cold Spring Harb Perspect Biol 7, doi: 10.1101/cshperspect.a021303 (2015).
31. Hunter, R. G., Gagnidze, K., McEwen, B. S. & Pfaff, D. W. Stress and the dynamic genome: Steroids, epigenetics, and the transposome. Proc Natl Acad Sci USA 112, 6828-6833, doi: 10.1073/pnas.1411260111 (2015).
32. Lucassen, P. J. et al. Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets 5, 531-546 (2006).
33. Snyder, J. S., Soumier, A., Brewer, M., Pickel, J. & Cameron, H. A. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476, 458-461, doi: 10.1038/nature10287 (2011).
34. Opendak, M. & Gould, E. New neurons maintain efficient stress recovery. Cell Stem Cell 9, 287-288, doi: 10.1016/j.stem.2011.09.003 (2011).
35. Samson, J. et al. Noise-induced time-dependent changes in oxidative stress in the mouse cochlea and attenuation by D-methionine. Neuroscience 152, 146-150, doi:10.1016/j.neuroscience.2007.11.015 (2008).
36. Sarah Hayes, S. M., Brian Allman & Richard Salvi. Stress Hormone Levels and Hippocampal Neurogenesis Following Acoustic Trauma in The 34th Annual Midwinter meeting of Association For Research in Otolaryngology. Baltimore, USA. Association For Research in Otolaryngology (2011).
37. Zheng, Y., Hamilton, E., Begum, S., Smith, P. F. & Darlington, C. L. The effects of acoustic trauma that can cause tinnitus on spatial performance in rats. Neuroscience 186, 48-56, doi: 10.1016/j.neuroscience.2011.04.052 (2011).
38. Lin, F. R. et al. Hearing loss and incident dementia. Arch Neurol 68, 214-220, doi: 68/2/21410.1001/archneurol.2010.362 (2011).
39. Lin, F. R. et al. Hearing loss and cognition in the Baltimore Longitudinal Study of Aging. Neuropsychology 25, 763-770, doi: 2011-13415-001 10.1037/a0024238 (2011).
40. Lin, F. R. Hearing loss and cognition among older adults in the United States. J Gerontol A Biol Sci Med Sci 66, 1131-1136, doi: 10.1093/gerona/glr115 glr115 (2011).
41. Lin, F. R. et al. Hearing Loss and Cognitive Decline in Older Adults. JAMA Intern Med. 1-7, doi: 1558452 10.1001/jamainternmed.2013.1868 (2013).
42. Moxon, K. A. et al. Multiple single units and population responses during inhibitory gating of hippocampal auditory response in freely-moving rats. Brain Res 825, 75-85 (1999).
43. O'Mara, S. The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. J Anat 207, 271-282, doi: 10.1111/j.1469-7580.2005.00446.x (2005).
44. Shi, L. et al. Ribbon synapse plasticity in the cochleae of Guinea pigs after noise-induced silent damage. PLoS One 8, e81566, doi: 10.1371/journal.pone.0081566 PONE-D-13-30022 (2013).
45. Liu, L. et al. Silent damage of noise on cochlear afferent innervation in guinea pigs and the impact on temporal processing. PLoS One 7, e49550, doi: 10.1371/journal.pone.0049550 PONE-D-12-26008 (2012).
46. Kujawa, S. G. & Liberman, M. C. Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J Neurosci 29, 14077-14085, doi: 29/45/14077 10.1523/JNEUROSCI.2845-09.2009 (2009).
47. Kim, H. et al. Influence of prenatal noise and music on the spatial memory and neurogenesis in the hippocampus of developing rats. Brain Dev 28, 109-114, doi:10.1016/j.braindev.2005.05.008 (2006).
48. Curlik, D. M. 2nd, Maeng, L. Y., Agarwal, P. R. & Shors, T. J. Physical skill training increases the number of surviving new cells in the adult hippocampus. PLoS One 8, e55850, doi: 10.1371/journal.pone.0055850 PONE-D-12-21761 (2013).
49. Xu, Z. et al. Working memory task decreases the survival of newly born neurons in hippocampus. Neurobiol Learn Mem 95, 239-247, doi: S1074-7427(10)00199-1 10.1016/j.nlm.2010.11.013 (2011).
50. Anderson, M. L., Sisti, H. M., Curlik, D. M. 2nd & Shors, T. J. Associative learning increases adult neurogenesis during a critical period. Eur J Neurosci 33, 175-181, doi: 10.1111/j.1460-9568.2010.07486.x (2011).
51. Cameron, H. A. & McKay, R. D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435, 406-417 (2001).
52. Attardo, A. et al. Tis21 expression marks not only populations of neurogenic precursor cells but also new postmitotic neurons in adult hippocampal neurogenesis. Cerebral cortex 20, 304-314, doi: 10.1093/cercor/bhp100 (2010).
53. Veyrac, A. et al. Zif268/egr1 gene controls the selection, maturation and functional integration of adult hippocampal newborn neurons by learning. Proc Natl Acad Sci USA 110, 7062-7067, doi: 1220558110 10.1073/pnas.1220558110 (2013).
54. Epp, J. R., Chow, C. & Galea, L. A. Hippocampus-dependent learning influences hippocampal neurogenesis. Front Neurosci 7, 57, doi: 10.3389/fnins.2013.00057 (2013).
55. Gould, E., Beylin, A., Tanapat, P., Reeves, A. & Shors, T. J. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2, 260-265, doi: 10.1038/6365 (1999).
56. Kohler, S. J., Williams, N. I., Stanton, G. B., Cameron, J. L. & Greenough, W. T. Maturation time of new granule cells in the dentate gyrus of adult macaque monkeys exceeds six months. Proc Natl Acad Sci USA 108, 10326-10331, doi: 10.1073/pnas.1017099108 (2011).
57. Bruno, S. & Darzynkiewicz, Z. Cell cycle dependent expression and stability of the nuclear protein detected by Ki-67 antibody in HL-60 cells. Cell proliferation 25, 31-40 (1992).
58. Wang, J. et al. Overexpression of X-linked inhibitor of apoptosis protein protects against noise-induced hearing loss in mice. Gene Ther 18, 560-568, doi: gt2010172 10.1038/gt.2010.172 (2011).
59. Mendez-Couz, M., Conejo, N. M., Vallejo, G. & Arias, J. L. Spatial memory extinction: A c-Fos protein mapping study. Behav Brain Res 260, 101-110, doi: 10.1016/j.bbr.2013.11.032 S0166-4328(13)00719-5 (2014).
60. Bonaccorsi, J. et al. System consolidation of spatial memories in mice: effects of enriched environment. Neural Plast 2013, 956312, doi: 10.1155/2013/956312 (2013).
61. Vorhees, C. V. & Williams, M. T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1, 848-858, doi: nprot.2006.116 10.1038/nprot.2006.116 (2006).