Blast-induced hearing loss suppresses hippocampal neurogenesis and disrupts long term spatial memory

Alattar, 2020, Hearing impairment and cognitive decline in older, community-dwelling adults, J. Gerontol. A Biol. Sci. Med. Sci., 75, 567, 10.1093/gerona/glz035 Altman, 1965, Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats, J. Comp. Neurol., 124, 319, 10.1002/cne.901240303 Anchan, 2014, GPR30 activation decreases anxiety in the open field test but not in the elevated plus maze test in female mice, Brain Behav., 4, 51, 10.1002/brb3.197 Aronov, 2017, Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit, Nature, 543, 719, 10.1038/nature21692 Arslan, 2018, Anxiety and depression in patients with sudden one-sided hearing loss, Ear Nose Throat J., 97, E7, 10.1177/0145561318097010-1101 Awwad, 2015, Blast overpressure waves induce transient anxiety and regional changes in cerebral glucose metabolism and delayed hyperarousal in rats, Front. Neurol., 6, 132, 10.3389/fneur.2015.00132 Baizer, 2015, Effects of acoustic trauma on the auditory system of the rat: the role of microglia, Neuroscience, 303, 299, 10.1016/j.neuroscience.2015.07.004 Brandeis, 1989, The use of the Morris Water Maze in the study of memory and learning, Int. J. Neurosci., 48, 29, 10.3109/00207458909002151 Brown, 2003, Transient expression of doublecortin during adult neurogenesis, J. Comp. Neurol., 467, 1, 10.1002/cne.10874 Calford, 1993, Rapid changes in frequency tuning of neurons in cat auditory cortex resulting from pure-tone-induced temporary threshold shift, Neuroscience, 55, 953, 10.1016/0306-4522(93)90310-C Cameron, 1994, Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus, Neuroscience, 61, 203, 10.1016/0306-4522(94)90224-0 Chan, 2017, Interaction effect of social isolation and high dose corticosteroid on neurogenesis and emotional behavior, Front. Behav. Neurosci., 11, 18, 10.3389/fnbeh.2017.00018 Chen, 2010, Too much of a good thing: long-term treatment with salicylate strengthens outer hair cell function but impairs auditory neural activity, Hear. Res., 265, 63, 10.1016/j.heares.2010.02.010 Chen, 2015, Tinnitus and hyperacusis involve hyperactivity and enhanced connectivity in auditory-limbic-arousal-cerebellar network, Elife, 4, 10.7554/eLife.06576 Church, 1988, The neuroprotective action of ketamine and MK-801 after transient cerebral ischemia in rats, Anesthesiology, 69, 702, 10.1097/00000542-198811000-00011 Clarke, 2017, Ketamine modulates hippocampal neurogenesis and pro-inflammatory cytokines but not stressor induced neurochemical changes, Neuropharmacology, 112, 210, 10.1016/j.neuropharm.2016.04.021 Clelland, 2009, A functional role for adult hippocampal neurogenesis in spatial pattern separation, Science, 325, 210, 10.1126/science.1173215 Contrera, 2017, Association of hearing impairment and anxiety in older adults, J. Aging Health, 29, 172 Cooper, 2016, Memory and functional brain differences in a national sample of U.S. veterans with Gulf War illness, Psychiatry Res. Neuroimaging., 250, 33, 10.1016/j.pscychresns.2016.03.004 Cosh, 2018, The association amongst visual, hearing, and dual sensory loss with depression and anxiety over 6 years: the Tromso Study, Int. J. Geriatr. Psychiatr., 33, 598, 10.1002/gps.4827 Du, 2013, Effects of antioxidant treatment on blast-induced brain injury, PLoS One, 8, 10.1371/journal.pone.0080138 Du, 2017, Antioxidants reduce neurodegeneration and accumulation of pathologic Tau proteins in the auditory system after blast exposure, Free Radic. Biol. Med., 108, 627, 10.1016/j.freeradbiomed.2017.04.343 Eggermont, 2015, The auditory cortex and tinnitus - a review of animal and human studies, Eur. J. Neurosci., 41, 665, 10.1111/ejn.12759 Eriksson, 1998, Neurogenesis in the adult human hippocampus, Nat. Med., 4, 1313, 10.1038/3305 Feng, 2012, Degeneration in the ventral cochlear nucleus after severe noise damage in mice, J. Neurosci. Res., 90, 831, 10.1002/jnr.22793 Fenton, 2000, Conjoint control of hippocampal place cell firing by two visual stimuli. Ii. A vector-field theory that predicts modifications of the representation of the environment, J. Gen. Physiol., 116, 211, 10.1085/jgp.116.2.211 Fontana, 2006, Cell proliferation in the adult hippocampal formation of rodents and its modulation by entorhinal and fimbria-fornix afferents, Cerebr. Cortex, 16, 301, 10.1093/cercor/bhi120 Garinther, 1979, Impulse noise of army weapons, J. Acoust. Soc. Am., 65, 10.1121/1.2017190 Gehrmann, 1991, Lesion of the rat entorhinal cortex leads to a rapid microglial reaction in the dentate gyrus. A light and electron microscopical study, Acta Neuropathol., 82, 442, 10.1007/BF00293378 Gilbertson, 2001, Multivariate assessment of explicit memory function in combat veterans with posttraumatic stress disorder, J. Trauma Stress, 14, 413, 10.1023/A:1011181305501 Goble, 2009, Acute high-intensity sound exposure alters responses of place cells in hippocampus, Hear. Res., 253, 52, 10.1016/j.heares.2009.03.002 Goodman, 2010, Young hippocampal neurons are critical for recent and remote spatial memory in adult mice, Neuroscience, 171, 769, 10.1016/j.neuroscience.2010.09.047 Gurgel, 2014, Relationship of hearing loss and dementia: a prospective, population-based study, Otol. Neurotol., 35, 775, 10.1097/MAO.0000000000000313 Hamernik, 1984, Anatomical correlates of impulse noise-induced mechanical damage in the cochlea, Hear. Res., 13, 229, 10.1016/0378-5955(84)90077-7 Hayes, 2019, Noise-induced hearing loss alters hippocampal glucocorticoid receptor expression in rats, Hear. Res., 379, 43, 10.1016/j.heares.2019.04.013 Helfer, 2011, Noise-induced hearing injury and comorbidities among postdeployment U.S. Army soldiers: april 2003-June 2009, Am. J. Audiol., 20, 33, 10.1044/1059-0889(2011/10-0033) Huang, 2012, Redox balance- and radiation-mediated alteration in hippocampal neurogenesis, Free Radic. Res., 48, 951, 10.3109/10715762.2012.664770 Hufner, 2011, Spatial separation of visual and vestibular processing in the human hippocampal formation, Ann. N. Y. Acad. Sci., 1233, 177, 10.1111/j.1749-6632.2011.06115.x Jokel, 2019, Noise of military weapons, ground vehicles, planes and ships, J. Acoust. Soc. Am., 146, 3832, 10.1121/1.5134069 Jung, 1993, Spatial selectivity of unit activity in the hippocampal granular layer, Hippocampus, 3, 165, 10.1002/hipo.450030209 Karr, 2014, Blast-related mild traumatic brain injury: a Bayesian random-effects meta-analysis on the cognitive outcomes of concussion among military personnel, Neuropsychol. Rev., 24, 428, 10.1007/s11065-014-9271-8 Kohman, 2013, Neurogenesis, inflammation and behavior, Brain Behav. Immun., 27, 22, 10.1016/j.bbi.2012.09.003 Kraus, 2012, Neuronal connectivity and interactions between the auditory and limbic systems. Effects of noise and tinnitus, Hear. Res., 288, 34, 10.1016/j.heares.2012.02.009 Kraus, 2010, Noise trauma impairs neurogenesis in the rat hippocampus, Neuroscience, 167, 1216, 10.1016/j.neuroscience.2010.02.071 Lesicko, 2016, Connectional modularity of top-down and bottom-up multimodal inputs to the lateral cortex of the mouse inferior colliculus, J. Neurosci., 36, 11037, 10.1523/JNEUROSCI.4134-15.2016 Limoli, 2004, Radiation response of neural precursor cells: linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress, Radiat. Res., 161, 17, 10.1667/RR3112 Lin, 2011, Hearing loss and cognition in the baltimore longitudinal study of aging, Neuropsychology, 25, 763, 10.1037/a0024238 Lin, 2011, Primary neural degeneration in the Guinea pig cochlea after reversible noise-induced threshold shift, J. Assoc. Res. Otolaryngol., 12, 605, 10.1007/s10162-011-0277-0 Liu, 2019, Association of hearing loss with dementia, JAMA Network Open, 2, 10.1001/jamanetworkopen.2019.8112 Liu, 2018, Hippocampal mechanisms underlying impairment in spatial learning long after establishment of noise-induced hearing loss in CBA mice, Front. Syst. Neurosci., 12, 35, 10.3389/fnsys.2018.00035 Liu, 2016, Noise induced hearing loss impairs spatial learning/memory and hippocampal neurogenesis in mice, Sci. Rep., 6 Lucassen, 2015, Regulation of adult neurogenesis and plasticity by (early) stress, glucocorticoids, and inflammation, Cold Spring Harb. Perspect. Biol., 7, 10.1101/cshperspect.a021303 Lucassen, 2006, Stress, depression and hippocampal apoptosis, CNS Neurol. Disord. - Drug Targets, 5, 531, 10.2174/187152706778559273 Madsen, 2003, Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat, Neuroscience, 119, 635, 10.1016/S0306-4522(03)00199-4 Manohar, 2011, 431 Manohar, 2012, Expression of doublecortin, a neuronal migration protein, in unipolar brush cells of the vestibulocerebellum and dorsal cochlear nucleus of the adult rat, Neuroscience, 202, 169, 10.1016/j.neuroscience.2011.12.013 McDermott, 2016, Male veterans with PTSD exhibit aberrant neural dynamics during working memory processing: an MEG study, J. Psychiatry Neurosci., 41, 251, 10.1503/jpn.150058 McIntosh, 1998, Large-scale functional connectivity in associative learning: interrelations of the rat auditory, visual, and limbic systems, J. Neurophysiol., 80, 3148, 10.1152/jn.1998.80.6.3148 McNaughton, 1989, Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge, Exp. Brain Res., 76, 485, 10.1007/BF00248904 Michler, 2002, Acoustic trauma induces reemergence of the growth- and plasticity-associated protein GAP-43 in the rat auditory brainstem, J. Comp. Neurol., 451, 250, 10.1002/cne.10348 Mohan, 2018, Distress-dependent temporal variability of regions encoding domain-specific and domain-general behavioral manifestations of phantom percepts, Eur. J. Neurosci., 48, 1743, 10.1111/ejn.13988 Morest, 1983, Noise-induced degeneration in the brain and representation of inner and outer hair cells, Hear. Res., 9, 145, 10.1016/0378-5955(83)90024-2 Morris, 1984, Developments of a water-maze procedure for studying spatial learning in the rat, J. Neurosci. Methods, 11, 47, 10.1016/0165-0270(84)90007-4 Moser, 2014, Network mechanisms of grid cells, Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 10.1098/rstb.2012.0511 Mosnier, 2015, Improvement of cognitive function after cochlear implantation in elderly patients, JAMA Otolaryngol. Head Neck. Surg., 141, 442, 10.1001/jamaoto.2015.129 Munoz-Lopez, 2010, Anatomical pathways for auditory memory in primates, Front. Neuroanat., 4, 129, 10.3389/fnana.2010.00129 Newman, 2015, Low-cost blast wave generator for studies of hearing loss and brain injury: blast wave effects in closed spaces, J. Neurosci. Methods, 242, 82, 10.1016/j.jneumeth.2015.01.009 Oitzl, 1998, Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats, Eur. J. Neurosci., 10, 3759, 10.1046/j.1460-9568.1998.00381.x Oomen, 2007, Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress, Eur. J. Neurosci., 26, 3395, 10.1111/j.1460-9568.2007.05972.x Paolone, 2011 Pascual, 2015, Large-scale brain networks of the human left temporal pole: a functional connectivity MRI study, Cerebr. Cortex, 25, 680, 10.1093/cercor/bht260 Proescholdt, 2001, Neuroprotection of S(+) ketamine isomer in global forebrain ischemia, Brain Res., 904, 245, 10.1016/S0006-8993(01)02465-9 Raber, 2004, Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis, Radiat. Res., 162, 39, 10.1667/RR3206 Ravassard, 2013, Multisensory control of hippocampal spatiotemporal selectivity, Science, 340, 1342, 10.1126/science.1232655 Risling, 2011, Mechanisms of blast induced brain injuries, experimental studies in rats, Neuroimage, 54, S89, 10.1016/j.neuroimage.2010.05.031 Robertson, 2013, Spontaneous hyperactivity in the auditory midbrain: relationship to afferent input, Hear. Res., 295, 124, 10.1016/j.heares.2012.02.002 Rola, 2004, Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice, Exp. Neurol., 188, 316, 10.1016/j.expneurol.2004.05.005 Saaltink, 2014, Stress, glucocorticoid receptors, and adult neurogenesis: a balance between excitation and inhibition?, Cell. Mol. Life Sci., 71, 2499, 10.1007/s00018-014-1568-5 Sandi, 2007, Stress and memory: behavioral effects and neurobiological mechanisms, Neural Plast., 2007, 10.1155/2007/78970 Scott, 2000, Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures, Exp. Neurol., 165, 231, 10.1006/exnr.2000.7458 Scotto-Lomassese, 2002, Sensory inputs stimulate progenitor cell proliferation in an adult insect brain, Curr. Biol., 12, 1001, 10.1016/S0960-9822(02)00889-8 Sheppard, 2017, Prolonged low-level noise-induced plasticity in the peripheral and central auditory system of rats, Neuroscience, 359, 159, 10.1016/j.neuroscience.2017.07.005 Shively, 2012, Traumatic brain injury, shell shock, and posttraumatic stress disorder in the military--past, present, and future, J. Head Trauma Rehabil., 27, 234, 10.1097/HTR.0b013e318250e9dd Shors, 2002, Neurogenesis may relate to some but not all types of hippocampal-dependent learning, Hippocampus, 12, 578, 10.1002/hipo.10103 Shors, 2001, Neurogenesis in the adult is involved in the formation of trace memories, Nature, 410, 372, 10.1038/35066584 Shukla, 2019, Attenuation of adverse effects of noise induced hearing loss on adult neurogenesis and memory in rats by intervention with Adenosine A2A receptor agonist, Brain Res. Bull., 147, 47, 10.1016/j.brainresbull.2019.02.006 Sidor, 2010, Validation of an automated system for measuring anxiety-related behaviours in the elevated plus maze, J. Neurosci. Methods, 188, 7, 10.1016/j.jneumeth.2010.01.021 Sierra, 2010, Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis, Cell Stem Cell, 7, 483, 10.1016/j.stem.2010.08.014 Snyder, 2005, A role for adult neurogenesis in spatial long-term memory, Neuroscience, 130, 843, 10.1016/j.neuroscience.2004.10.009 Sweatt, 2004, Hippocampal function in cognition, Psychopharmacology (Berlin), 174, 99, 10.1007/s00213-004-1795-9 Szczepaniak, 1996, Evidence of neuronal plasticity within the inferior colliculus after noise exposure: a study of evoked potentials in the rat, Electroencephalogr. Clin. Neurophysiol., 100, 158, 10.1016/0013-4694(95)00234-0 Tamura, 1992, Monkey hippocampal neuron responses to complex sensory stimulation during object discrimination, Hippocampus, 2, 287, 10.1002/hipo.450020308 Tamura, 1992, Spatial responsiveness of monkey hippocampal neurons to various visual and auditory stimuli, Hippocampus, 2, 307, 10.1002/hipo.450020309 Tea, 2019, Social stress increases plasma cortisol and reduces forebrain cell proliferation in subordinate male zebrafish (Danio rerio), J. Exp. Biol., 222, 10.1242/jeb.194894 Tischler, 2006, The relationship between hippocampal volume and declarative memory in a population of combat veterans with and without PTSD, Ann. N. Y. Acad. Sci., 1071, 405, 10.1196/annals.1364.031 Van Bokhoven, 2011, Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment, Eur. J. Neurosci., 33, 1833, 10.1111/j.1460-9568.2011.07668.x Vetter, 2002, Urocortin-deficient mice show hearing impairment and increased anxiety-like behavior, Nat. Genet., 31, 363, 10.1038/ng914 Whitney, 2009, Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders, J. Neurochem., 108, 1343, 10.1111/j.1471-4159.2009.05886.x Winocur, 2006, Inhibition of neurogenesis interferes with hippocampus-dependent memory function, Hippocampus, 16, 296, 10.1002/hipo.20163 Xu, 2016, Disrupted functional brain connectome in unilateral sudden sensorineural hearing loss, Hear. Res., 335, 138, 10.1016/j.heares.2016.02.016 Yang, 2018, Altered brain functional connectome in migraine with and without restless legs syndrome: a resting-state functional MRI study, Front. Neurol., 9, 25, 10.3389/fneur.2018.00025 Zheng, 2001, Damage to the vestibular inner ear causes long-term changes in neuronal nitric oxide synthase expression in the rat hippocampus, Neuroscience, 105, 1, 10.1016/S0306-4522(01)00217-2 Zuckerman, 2019, Role of endogenous and exogenous corticosterone on behavioral and cognitive responses to low-pressure blast wave exposure, J. Neurotrauma, 36, 380, 10.1089/neu.2018.5672 Zuo, 2011, RU486 (mifepristone) ameliorates cognitive dysfunction and reverses the down-regulation of astrocytic N-myc downstream-regulated gene 2 in streptozotocin-induced type-1 diabetic rats, Neuroscience, 190, 156, 10.1016/j.neuroscience.2011.06.025