Abstract
Central nervous system (CNS) development is a very complex process that can be altered by environmental stimuli such as noise, which can generate long-term auditory and/or extra-auditory impairments. We have previously reported that early noise exposure can induce hippocampus-related behavioral alterations in postnatal day (PND) 28 adolescent rats. Furthermore, we recently found biochemical modifications in the hippocampus (HC) of these animals that seemed to endure even in more mature animals (i.e. PND35) and that have not been studied along with behavioral correlates. Thus, the aim of this work was to reveal novel data about the effects of early noise exposure on hippocampal-dependent behaviors in more mature animals. Additionally, extended enriched environment (EE) housing was evaluated to determine its capacity to induce behavioral modifications, either by its neuroprotective ability or the greater stimulation that it generates. Male Wistar rats were exposed to different noise schemes at PND7 or PND15. Upon weaning, some animals were transferred to EE whereas others were kept in standard cages. At PND35, different hippocampal-dependent behavioral assessments were performed. Results showed noise-induced behavioral changes that differed according to the scheme and age of exposure used. In addition, housing in an EE was effective either in preventing some of these changes or in inducing the appearance of new behavioral modifications. These findings suggest that CNS development would be sensitive to the effects of different type of environmental stimuli such as noise or enriched housing, leading to maladaptive behavioral changes that last even until adolescence.
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The data that support the findings of this study are available on request from the corresponding author SJM.
Abbreviations
- CNS:
-
Central nervous system
- EE:
-
Enriched environment
- EPM:
-
Elevated plus maze
- HC:
-
Hippocampus
- IA:
-
Inhibitory avoidance
- N1/N5:
-
Exposure schemes: 1 day and 5 days, respectively
- OF:
-
Open field
- PND7:
-
Rats exposed to noise at 7 days of age
- PND15:
-
Rats exposed to noise at 15 days of age
- ROS:
-
Reactive oxygen species
- St:
-
Standard cage
References
Alimohammadi I, Ahmadi Kanrash F, Abolghasemi J et al (2018) Effect of chronic noise exposure on aggressive behavior of automotive industry workers. Int J Occup Environ Med 9:170–175. https://doi.org/10.15171/ijoem.2018.1375
Alvarado JC, Fuentes-Santamaría V, Melgar-Rojas P et al (2015) Synergistic effects of free radical scavengers and cochlear vasodilators: a new otoprotective strategy for age-related hearing loss. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2015.00086
Angrini MA, Leslie JC (2012) Vitamin C attenuates the physiological and behavioural changes induced by long-term exposure to noise. Behav Pharmacol. https://doi.org/10.1097/FBP.0b013e32834f9f68
Atucha E, Roozendaal B (2015) The inhibitory avoidance discrimination task to investigate accuracy of memory. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2015.00060
Avishai-Eliner S, Brunson KL, Sandman CA, Baram TZ (2002) Stressed-out, or in (utero)? Trends Neurosci 25:518–524
Azman KF, Zakaria R, Abdaziz C et al (2015) Tualang honey improves memory performance and decreases depressive-like behavior in rats exposed to loud noise stress. Noise Health. https://doi.org/10.4103/1463-1741.153388
Badache S, Bouslama S, Brahmia O et al (2017) Prenatal noise and restraint stress interact to alter exploratory behavior and balance in juvenile rats, and mixed stress reverses these effects. Stress 20:320–328. https://doi.org/10.1080/10253890.2017.1307962
Bannerman DM, Rawlins JNP, McHugh SB et al (2004) Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev 28:273–283
Baraldi T, Schöwe NM, Balthazar J et al (2013) Cognitive stimulation during lifetime and in the aged phase improved spatial memory, and altered neuroplasticity and cholinergic markers of mice. Exp Gerontol. https://doi.org/10.1016/j.exger.2013.05.055
Barrientos RM, Higgins EA, Sprunger DB et al (2002) Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration. Behav Brain Res. https://doi.org/10.1016/S0166-4328(02)00045-1
Barros D, Amaral OB, Izquierdo I et al (2006) Behavioral and genoprotective effects of Vaccinium berries intake in mice. Pharmacol Biochem Behav. https://doi.org/10.1016/j.pbb.2006.05.001
Beery AK (2018) Inclusion of females does not increase variability in rodent research studies. Curr Opin Behav Sci 23:143–149. https://doi.org/10.1016/j.cobeha.2018.06.016
Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728–739
Benaroya-Milshtein N, Hollander N, Apter A et al (2004) Environmental enrichment in mice decreases anxiety, attenuates stress responses and enhances natural killer cell activity. Eur J Neurosci. https://doi.org/10.1111/j.1460-9568.2004.03587.x
Bendix I, Weichelt U, Strasser K et al (2012) Hyperoxia changes the balance of the thioredoxin/peroxiredoxin system in the neonatal rat brain. Brain Res. https://doi.org/10.1016/j.brainres.2012.09.024
Bureš Z, Grécová J, Popelář J, Syka J (2010) Noise exposure during early development impairs the processing of sound intensity in adult rats. Eur J Neurosci. https://doi.org/10.1111/j.1460-9568.2010.07280.x
Campeau S, Dolan D, Akil H, Watson SJ (2002) c-fos mRNA induction in acute and chronic audiogenic stress: possible role of the orbitofrontal cortex in habituation. Stress 5:121–130. https://doi.org/10.1080/10253890290027895
Carobrez AP, Bertoglio LJ (2005) Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. In: Neuroscience and biobehavioral reviews 29(8), 1193–1205. https://doi.org/10.1016/j.neubiorev.2005.04.017
Cheng L, Wang SH, Chen QC, Liao XM (2011) Moderate noise induced cognition impairment of mice and its underlying mechanisms. Physiol Behav. https://doi.org/10.1016/j.physbeh.2011.06.018
Cheng L, Wang SH, Huang Y, Liao XM (2016) The hippocampus may be more susceptible to environmental noise than the auditory cortex. Hear Res. https://doi.org/10.1016/j.heares.2016.01.001
Clark C, Crombie R, Head J et al (2012) Does traffic-related air pollution explain associations of aircraft and road traffic noise exposure on children’s health and cognition? A secondary analysis of the United Kingdom sample from the RANCH project. Am J Epidemiol. https://doi.org/10.1093/aje/kws012
Clayton JA, Collins FS (2014) Policy: NIH to balance sex in cell and animal studies. Nature 509:282–283. https://doi.org/10.1038/509282a
Crofton EJ, Zhang Y, Green TA (2015) Inoculation stress hypothesis of environmental enrichment. Neurosci Biobehav Rev 49:19–31
Cui B, Li K (2013) Chronic noise exposure and Alzheimer disease: is there an etiological association? Med Hypotheses. https://doi.org/10.1016/j.mehy.2013.07.017
Cui B, Wu M, She X (2009) Effects of chronic noise exposure on spatial learning and memory of rats in relation to neurotransmitters and NMDAR2B alteration in the hippocampus. J Occup Health. https://doi.org/10.1539/joh.L8084
Ennaceur A (2014) Tests of unconditioned anxiety—pitfalls and disappointments. Physiol Behav 135:55–71
Evans GW, Lercher P, Meis M et al (2001) Community noise exposure and stress in children. J Acoust Soc Am. https://doi.org/10.1121/1.1340642
Fanselow MS (2000) Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110(1–2):73–81. https://doi.org/10.1016/s0166-4328(99)00186-2
Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19
Farooqui T, Farooqui AA (2009) Aging: an important factor for the pathogenesis of neurodegenerative diseases. Mech Ageing Dev. https://doi.org/10.1016/j.mad.2008.11.006
Fernández-Quezada D, Moran-Torres D, Luquin S et al (2019) Male/female differences in radial arm water maze execution after chronic exposure to noise. Noise Health 21:25–34. https://doi.org/10.4103/nah.NAH_23_19
Friske JE, Gammie SC (2005) Environmental enrichment alters plus maze, but not maternal defense performance in mice. Physiol Behav. https://doi.org/10.1016/j.physbeh.2005.03.022
Fujimoto C, Yamasoba T (2014) Oxidative stresses and mitochondrial dysfunction in age-related hearing loss. Oxid Med Cell Longev, 2014, 582849. https://doi.org/10.1155/2014/582849
Golbidi S, Li H, Laher I (2018) Oxidative stress: a unifying mechanism for cell damage induced by noise, (water-pipe) smoking, and emotional stress—therapeutic strategies targeting redox imbalance. Antioxid Redox Signal 28:741–759
Grigoryan G, Segal M (2016) Lasting differential effects on plasticity induced by prenatal stress in dorsal and ventral hippocampus. Neural Plast, 2016, 2540462. https://doi.org/10.1155/2016/2540462
Hahad O, Prochaska JH, Daiber A, Muenzel T (2019) Environmental noise-induced effects on stress hormones, oxidative stress, and vascular dysfunction: key factors in the relationship between cerebrocardiovascular and psychological disorders. Oxid Med Cell Longev 2019:4623109. https://doi.org/10.1155/2019/4623109
Ismail FY, Fatemi A, Johnston MV (2017) Cerebral plasticity: windows of opportunity in the developing brain. Eur J Paediatr Neurol 21:23–48
Izquierdo I, Medina JH (1997) Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem. https://doi.org/10.1006/nlme.1997.3799
Izquierdo I, Furini CRG, Myskiw JC (2016) Fear memory. Physiol Rev. https://doi.org/10.1152/physrev.00018.2015
Jafari Z, Kolb BE, Mohajerani MH (2018) Chronic traffic noise stress accelerates brain impairment and cognitive decline in mice. Exp Neurol 308:1–12. https://doi.org/10.1016/j.expneurol.2018.06.011
Jáuregui-Huerta F, García-Estrada J, Ruvalcaba-Delgadillo Y et al (2011) Chronic exposure of juvenile rats to environmental noise impairs hippocampal cell proliferation in adulthood. Noise Health. https://doi.org/10.4103/1463-1741.82961
Kazi AI, Oommen A (2014) Chronic noise stress-induced alterations of glutamate and gamma-aminobutyric acid and their metabolism in the rat brain. Noise Health. https://doi.org/10.4103/1463-1741.144394
Kim M, Chang SI, Seong JC et al (2012) Road traffic noise: annoyance, sleep disturbance, and public health implications. Am J Prev Med. https://doi.org/10.1016/j.amepre.2012.06.014
Kjelstrup KG, Tuvnes FA, Steffenach HA et al (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.152112399
Kolb B, Mychasiuk R, Gibb R (2014) Brain development, experience, and behavior. Pediatr Blood Cancer 61(10), 1720–1723. https://doi.org/10.1002/pbc.24908
Kraus KS, Mitra S, Jimenez Z et al (2010) Noise trauma impairs neurogenesis in the rat hippocampus. Neuroscience. https://doi.org/10.1016/j.neuroscience.2010.02.071
Kyriakou EI, Manfré G, Spadaro JA et al (2017) Anxiety and risk assessment-related traits in a rat model of Spinocerebellar ataxia type 17. Behav Brain Res. https://doi.org/10.1016/j.bbr.2016.12.023
Kyzar EJ, Floreani C, Teppen TL, Pandey SC (2016) Adolescent alcohol exposure: burden of epigenetic reprogramming, synaptic remodeling, and adult psychopathology. Front Neurosci 10:222
Laviola G, Hannan AJ, Macrì S et al (2008) Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31:159–168
Lee SL, Lew D, Wickenheisser V, Markus EJ (2019) Interdependence between dorsal and ventral hippocampus during spatial navigation. Brain Behav. https://doi.org/10.1002/brb3.1410
Lees B, Meredith LR, Kirkland AE et al (2020) Effect of alcohol use on the adolescent brain and behavior. Pharmacol Biochem Behav 192:172906
Leuner B, Gould E (2010) Structural plasticity and hippocampal function. Annu Rev Psychol. https://doi.org/10.1146/annurev.psych.093008.100359
Leussis MP, Bolivar VJ (2006) Habituation in rodents: a review of behavior, neurobiology, and genetics. Neurosci Biobehav Rev 30:1045–1064
Li K, Jia H, She X et al (2014) Role of NMDA receptors in noise-induced tau hyperphosphorylation in rat hippocampus and prefrontal cortex. J Neurol Sci. https://doi.org/10.1016/j.jns.2014.03.027
Lim J, Kweon K, Kim H-W et al (2018) Negative impact of noise and noise sensitivity on mental health in childhood. Noise Health 20:199–211. https://doi.org/10.4103/nah.NAH_9_18
Lima APAS, Silva K, Padovan CM et al (2014) Memory, learning, and participation of the cholinergic system in young rats exposed to environmental enrichment. Behav Brain Res. https://doi.org/10.1016/j.bbr.2013.10.046
Liu L, Shen P, He T et al (2016) Noise induced hearing loss impairs spatial learning/memory and hippocampal neurogenesis in mice. Sci Rep. https://doi.org/10.1038/srep20374
Liu L, Xuan C, Shen P et al (2018) Hippocampal mechanisms underlying impairment in spatial learning long after establishment of noise-induced hearing loss in CBA mice. Front Syst Neurosci 12:35. https://doi.org/10.3389/fnsys.2018.00035
Llorente R, Villa P, Marco EM, Viveros MP (2012) Analyzing the effects of a single episode of neonatal maternal deprivation on metabolite profiles in rat brain: a proton nuclear magnetic resonance spectroscopy study. Neuroscience. https://doi.org/10.1016/j.neuroscience.2011.11.033
Lores-Arnaiz S, Bustamante J, Arismendi M et al (2006) Extensive enriched environments protect old rats from the aging dependent impairment of spatial cognition, synaptic plasticity and nitric oxide production. Behav Brain Res. https://doi.org/10.1016/j.bbr.2006.01.016
Lyst SJ, Davis K, Gigg J, Hager R (2012) Effects of increased spatial complexity on behavioural development and task performance in lister hooded rats. PLoS ONE. https://doi.org/10.1371/journal.pone.0047640
Mahmoud S, Gharagozloo M, Simard C, Gris D (2019) Astrocytes maintain glutamate homeostasis in the CNS by controlling the balance between glutamate uptake and release. Cells. https://doi.org/10.3390/cells8020184
Manikandan S, Padma MK, Srikumar R et al (2006) 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. https://doi.org/10.1016/j.neulet.2006.01.037
Manukyan AL, Grigoryan AS, Hunanyan LS et al (2020) Alfa2-adrenoblockers attenuate the elevated plasma cholesterol, anxiety levels and restore impaired spatial memory of rats under the chronic noise exposure. Sci Total Environ 740:140390. https://doi.org/10.1016/j.scitotenv.2020.140390
McCreary JK, Metz GAS (2016) Environmental enrichment as an intervention for adverse health outcomes of prenatal stress. Environ Epigenet. https://doi.org/10.1093/eep/dvw013
McFarland, D., (1987). The Oxford Companion to Animal Behaviour. Oxford University Press, New York
McHugh SB, Deacon RMJ, Rawlins JNP, Bannerman DM (2004) Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav Neurosci. https://doi.org/10.1037/0735-7044.118.1.63
Mitra R, Sapolsky RM (2012) Short-term enrichment makes male rats more attractive, more defensive and alters hypothalamic neurons. PLoS ONE. https://doi.org/10.1371/journal.pone.0036092
Molina SJ, Guelman LR (2022) Noise-induced hippocampal damage: potential mechanisms. Neural Regen Res 17(3):563–564. https://doi.org/10.4103/1673-5374.320982
Molina SJ, Capani F, Guelman LR (2016a) Noise exposure of immature rats can induce different age-dependent extra-auditory alterations that can be partially restored by rearing animals in an enriched environment. Brain Res. https://doi.org/10.1016/j.brainres.2016.01.050
Molina SJ, Miceli M, Guelman LR (2016b) Noise exposure and oxidative balance in auditory and extra-auditory structures in adult and developing animals. Pharmacological approaches aimed to minimize its effects. Pharmacol Res. https://doi.org/10.1016/j.phrs.2015.11.022
Molina SJ, Buján GE, Rodriguez Gonzalez M et al (2019) Exposure of developing male rats to one or multiple noise sessions and different housing conditions: hippocampal thioredoxin changes and behavioral alterations. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2019.00182
Molina SJ, Buján GE, Guelman LR (2021) Noise-induced hippocampal oxidative imbalance and aminoacidergic neurotransmitters alterations in developing male rats: influence of enriched environment during adolescence. Dev Neurobiol. https://doi.org/10.1002/dneu.22806
Münzel T, Gori T, Babisch W, Basner M (2014) Cardiovascular effects of environmental noise exposure. Eur Heart J 35:829–836
Nadhimi Y, Llano DA (2020) Does hearing loss lead to dementia? A review of the literature. Hear Res. https://doi.org/10.1016/j.heares.2020.108038
Naqvi F, Haider S, Batool Z et al (2012) Sub-chronic exposure to noise affects locomotor activity and produces anxiogenic and depressive like behavior in rats. Pharmacol Rep. https://doi.org/10.1016/S1734-1140(12)70731-4
Nascimento Häckl LP, Carobrez AP (2007) Distinct ventral and dorsal hippocampus AP5 anxiolytic effects revealed in the elevated plus-maze task in rats. Neurobiol Learn Mem. https://doi.org/10.1016/j.nlm.2007.04.007
Nguyen D, Alavi MV, Kim KY et al (2011) A new vicious cycle involving glutamate excitotoxicity, oxidative stress and mitochondrial dynamics. Cell Death Dis. https://doi.org/10.1038/cddis.2011.117
NIOSH (1998) Occupational noise exposure. Natl Inst Occup Saf Health. https://doi.org/10.1038/clpt.2008.146
Nithianantharajah J, Hannan AJ (2006) Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697–709
O’keefe J, Nadel L (1979) Précis of O’Keefe & Nadel’s The hippocampus as a cognitive map. Behav Brain Sci. https://doi.org/10.1017/S0140525X00063949
Olaosun AO, Ogundiran O, Tobih JE (2009) Health hazards of noise: a review article. Res J Med Sci 3:115–122
Paw-Min-Thein-Oo SY, Kida H, Mitsushima D (2020) Proximodistal heterogeneity in learning-promoted pathway-specific plasticity at dorsal CA1 synapses. Neuroscience. https://doi.org/10.1016/j.neuroscience.2020.04.040
Pellow S, Chopin P, File SE, Briley M (1985) Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. https://doi.org/10.1016/0165-0270(85)90031-7
Pentkowski NS, Blanchard DC, Lever C et al (2006) Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur J Neurosci. https://doi.org/10.1111/j.1460-9568.2006.04754.x
Popović N, Caballero-Bleda M, Popović M (2014) Post-training scopolamine treatment induced maladaptive behavior in open field habituation task in rats. PLoS ONE. https://doi.org/10.1371/journal.pone.0100348
Pothuizen HHJ, Zhang WN, Jongen-Rêlo AL et al (2004) Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within-subject, within-task comparison of reference and working spatial memory. Eur J Neurosci. https://doi.org/10.1111/j.0953-816X.2004.03170.x
Rahimi O, Claiborne BJ (2007) Morphological development and maturation of granule neuron dendrites in the rat dentate gyrus. Prog Brain Res 163:167–181
Rodgers RJ, Cole JC (1993) Influence of social isolation, gender, strain, and prior novelty on plus-maze behaviour in mice. Physiol Behav. https://doi.org/10.1016/0031-9384(93)90084-S
Roozendaal B (2002) Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 78:578–595
Roy V, Chapillon P (2004) Further evidences that risk assessment and object exploration behaviours are useful to evaluate emotional reactivity in rodents. Behav Brain Res. https://doi.org/10.1016/j.bbr.2004.03.010
Rubio-Casillas A, Fernández-Guasti A (2016) The dose makes the poison: from glutamate-mediated neurogenesis to neuronal atrophy and depression. Rev Neurosci. https://doi.org/10.1515/revneuro-2015-0066
Ruvalcaba-Delgadillo Y, Luquín S, Ramos-Zúñiga R et al (2015) Early-life exposure to noise reduces mPFC astrocyte numbers and T-maze alternation/discrimination task performance in adult male rats. Noise Health. https://doi.org/10.4103/1463-1741.160703
Sakimoto Y, Mizuno J, Kida H et al (2019) Learning promotes subfield-specific synaptic diversity in hippocampal CA1 neurons. Cereb Cortex. https://doi.org/10.1093/cercor/bhz022
Sakurai Y (2002) Coding of auditory temporal and pitch information by hippocampal individual cells and cell assemblies in the rat. Neuroscience. https://doi.org/10.1016/S0306-4522(02)00509-2
Säljö A, Mayorga M, Bolouri H et al (2011) Mechanisms and pathophysiology of the low-level blast brain injury in animal models. Neuroimage. https://doi.org/10.1016/j.neuroimage.2010.05.050
Salomons AR, Arndt SS, Ohl F (2012) Impact of anxiety profiles on cognitive performance in BALB/c and 129P2 mice. Cogn Affect Behav Neurosci. https://doi.org/10.3758/s13415-012-0109-7
Sampedro-Piquero P, Begega A (2016) Environmental enrichment as a positive behavioral intervention across the lifespan. Curr Neuropharmacol. https://doi.org/10.2174/1570159x14666160325115909
Sasse SK, Greenwood BN, Masini CV et al (2008) Chronic voluntary wheel running facilitates corticosterone response habituation to repeated audiogenic stress exposure in male rats. Stress. https://doi.org/10.1080/10253890801887453
Schrijver NCA, Bahr NI, Weiss IC, Würbel H (2002) Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol Biochem Behav. https://doi.org/10.1016/S0091-3057(02)00790-6
Sies H (2015) Oxidative stress: a concept in redox biology and medicine. Redox Biol 4:180–183
Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev. https://doi.org/10.1016/S0149-7634(00)00014-2
Stansfeld S, Clark C (2015) Health effects of noise exposure in children. Curr Environ Health Rep 2:171–178
Stote DL, Fanselow MS (2004) NMDA receptor modulation of incidental learning in Pavlovian context conditioning. Behav Neurosci. https://doi.org/10.1037/0735-7044.118.1.253
Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15(10):655–669
Sundaramahalingam M, Ramasundaram S, Rathinasamy SD et al (2013) Role of Acorus calamus and α-asarone on hippocampal dependent memory in noise stress exposed rats. Pak J Biol Sci. https://doi.org/10.3923/pjbs.2013.770.778
Tamura H, Ohgami N, Yajima I et al (2012) Chronic exposure to low frequency noise at moderate levels causes impaired balance in mice. PLoS ONE. https://doi.org/10.1371/journal.pone.0039807
Tanaka KZ (2020) Heterogeneous representations in the hippocampus. Neurosci Res 165:1–5
Uran SL, Caceres LG, Guelman LR (2010) Effects of loud noise on hippocampal and cerebellar-related behaviors: role of oxidative state. Brain Res. https://doi.org/10.1016/j.brainres.2010.09.022
Uran SL, Aon-Bertolino ML, Caceres LG et al (2012) Rat hippocampal alterations could underlie behavioral abnormalities induced by exposure to moderate noise levels. Brain Res. https://doi.org/10.1016/j.brainres.2012.06.022
Uran SL, Gómez-Casati ME, Guelman LR (2014) Long-term recovery from hippocampal-related behavioral and biochemical abnormalities induced by noise exposure during brain development. Evaluation of auditory pathway integrity. Int J Dev Neurosci. https://doi.org/10.1016/j.ijdevneu.2014.06.002
van Kempen E, Fischer P, Janssen N et al (2012) Neurobehavioral effects of exposure to traffic-related air pollution and transportation noise in primary schoolchildren. Environ Res. https://doi.org/10.1016/j.envres.2012.03.002
van Praag H, Kempermann G, Gage FH (2000) Neural consequences of enviromental enrichment. Nat Rev Neurosci. https://doi.org/10.1038/35044558
Van Skike CE, Goodlett C, Matthews DB (2019) Acute alcohol and cognition: remembering what it causes us to forget. Alcohol 79:105–125
Vianna MRM, Alonso M, Viola H et al (2000) Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn Mem. https://doi.org/10.1101/lm.34600
Wald C, Wu C (2010) Of mice and women: the bias in animal models. Science (80-) 327:1571–1572. https://doi.org/10.1126/science.327.5973.1571
Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. https://doi.org/10.1038/nprot.2007.44
Wang S, Yu Y, Feng Y et al (2016) Protective effect of the orientin on noise-induced cognitive impairments in mice. Behav Brain Res. https://doi.org/10.1016/j.bbr.2015.09.024
Wankhar W, Srinivasan S, Rajan R, Sheeladevi R (2017) Antioxidant mediated response of Scoparia dulcis in noise-induced redox imbalance and immunohistochemical changes in rat brain. J Biomed Res. https://doi.org/10.7555/JBR.31.20150063
Weeden CSS, Roberts JM, Kamm AM, Kesner RP (2015) The role of the ventral dentate gyrus in anxiety-based behaviors. Neurobiol Learn Mem. https://doi.org/10.1016/j.nlm.2014.12.002
Yoon JH, Won JU, Lee W et al (2014) Occupational noise annoyance linked to depressive symptoms and suicidal ideation: a result from nationwide survey of Korea. PLoS One 9(8):e105321. https://doi.org/10.1371/journal.pone.0105321
Acknowledgements
We thank Marcela Vázquez, Eduardo Nieves and Enzo Cuba for their helpful assistance in the care of laboratory animals.
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This work was supported by the Universidad de Buenos Aires [20020160100005BA and 20020190100222BA]; Consejo Nacional de Investigaciones Científicas y Técnicas [PIP 00323]. SJM is a post-graduate CONICET fellowship and GEB is a post-graduate UBA fellowship.
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Molina, S.J., Lietti, Á.E., Carreira Caro, C.S. et al. Effects of early noise exposure on hippocampal-dependent behaviors during adolescence in male rats: influence of different housing conditions. Anim Cogn 25, 103–120 (2022). https://doi.org/10.1007/s10071-021-01540-1
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DOI: https://doi.org/10.1007/s10071-021-01540-1