Noise trauma impairs neurogenesis in the rat hippocampus

doi:10.1016/j.neuroscience.2010.02.071

Neuroscience

Volume 167, Issue 4, 2 June 2010, Pages 1216-1226

https://doi.org/10.1016/j.neuroscience.2010.02.071 Get rights and content

Abstract

The hippocampus, a major site of neurogenesis in the adult brain, plays an important role in memory. Based on earlier observations where exposure to high-intensity noise not only caused hearing loss but also impaired memory function, it is conceivably that noise exposure may suppress hippocampal neurogenesis. To evaluate this possibility, nine rats were unilaterally exposed for 2 h to a high-intensity, narrow band of noise centered at 12 kHz at 126 dB SPL. The rats were also screened for noise-induced tinnitus, a potential stressor which may suppress neurogenesis. Five rats developed persistent tinnitus-like behavior while the other four rats showed no signs of tinnitus. Age-matched sham controls showed no signs of hearing loss or tinnitus. The inner ear and hippocampus were evaluated for sensory hair cell loss and neurogenesis 10 weeks post-exposure. All noise exposed rats showed severe loss of sensory hair cells in the noise-exposed ear, but essentially no damage in the unexposed ear. Frontal sections from the hippocampus were immunolabeled for doublecortin to identify neuronal precursor cells, or Ki67 to label proliferating cells. Noise-exposed rats showed a significant reduction of neuronal precursors and fewer dividing cells as compared to sham controls. However, we could not detect any difference between rats with behavioral evidence of tinnitus versus rats without tinnitus. These results show for the first time that high intensity noise exposure not only damages the cochlea but also causes a significant and persistent decrease in hippocampal neurogenesis that may contribute to functional deficits in memory.

Section snippets

Animals

Twelve adult male Sprague–Dawley rats (Sasco, Charles River Laboratories International, Inc., Wilmington, MA, USA) were used for this study. Rats used for DCX and Ki67 immunolabeling were divided into two groups, Sham Controls (n=3) and Noise Trauma rats (n=9 for DCX staining and n=5 for Ki67 staining). To determine if noise trauma caused persistent changes in neurogenesis, Noise Trauma rats were unilaterally exposed to noise, screened for tinnitus, and sacrificed 10 weeks after noise exposure.

Inner ear damage after unilateral noise trauma

All rats unilaterally exposed to the 126 dB SPL noise showed nearly complete loss of OHC and IHC in the exposed ear between 20% and 100% distance from the apex of the cochlea (Fig. 2). This region corresponds roughly from 2 to >50 kHz on the rat cochlear frequency-place map (Müller, 1991, Greenwood, 1996). OHC loss extended further towards the apex than IHC. The pattern and extent of OHC and IHC damage showed relatively little variability across rats. Importantly, contralateral ears of all

Discussion

High intensity noise exposure has long been known to cause hearing loss by damaging the sensory hair cells and supporting cells in the inner ear (Bohne, 1977, Hamernik et al., 1984). However, much is still unknown about its effects on the CNS, particularly in regions outside the classical auditory pathway. Our results show for the first time that acoustic overstimulation (126 dB SPL, 2 h, 12 kHz) causes a long lasting suppression of hippocampal neurogenesis in adult rats. On average, the number

Conclusion

The results presented here are the first to demonstrate that noise exposure not only damages the peripheral auditory system, but also causes a major, long-term reduction of hippocampal neurogenesis. Thus, hearing protection or noise avoidance may not only protect the ear, but also the hippocampus, which is linked to memory and emotion. Because noise-induced hearing loss is extremely prevalent in industrialized societies, an important question that needs to be answered is what level of noise or

Acknowledgments

We thank Dr. Ison and Dr. Allen at the University at Rochester for generously sharing the custom software for startle reflex testing. This project was supported in part by grants from NIH (R01DC00909101; 1R01DC009219-01) and Tinnitus Research Initiative.

References (92)

S. Becker et al.
A model of hippocampal neurogenesis in memory and mood disorders
Trends Cogn Sci
(2007)
P.C. Bickford-Wimer et al.
Auditory sensory gating in hippocampal neurons: a model system in the rat
Biol Psychiatry
(1990)
S. Brene et al.
Running is rewarding and antidepressive
Physiol Behav
(2007)
H.A. Cameron et al.
Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat
Neuroscience
(1993)
F.T. Crews et al.
Neurogenesis in adolescent brain is potently inhibited by ethanol
Neuroscience
(2006)
D. Ding et al.
Ethacrynic acid rapidly and selectively abolishes blood flow in vessels supplying the lateral wall of the cochlea
Hear Res
(2002)
R.S. Duman
Depression: a case of neuronal life and death?
Biol Psychiatry
(2004)
C.L. Ehlers et al.
Long-latency event-related potentials in rats: effects of task and stimulus parameters
Neuroscience
(1994)
R.L. Folmer et al.
Tinnitus severity, loudness, and depression
Otolaryngol Head Neck Surg
(1999)
T.J. Goble et al.
Acute high-intensity sound exposure alters responses of place cells in hippocampus
Hear Res
(2009)

E. Gould et al.

Neurogenesis in adulthood: a possible role in learning

Trends Cogn Sci

(1999)

D. Greenwood

Comparing octaves, frequency ranges, and cochlear-map curvature across species

Hear Res

(1996)

J.B. Halford et al.

Anxiety and depression in tinnitus sufferers

J Psychosom Res

(1991)

R.P. Hamernik et al.

Anatomical correlates of impulse noise induced mechanical damage to the cochlear

Hear Res

(1984)

B. Hattiangady et al.

Chronic temporal lobe epilepsy is associated with severely declined dentate neurogenesis in the adult hippocampus

Neurobiol Dis

(2004)

J.S. Kim et al.

Differences in immunoreactivities of Ki67 and doublecortin in the adult hippocampus in three strains of mice

Acta Histochem

(2009)

R. Kuruba et al.

Hippocampal neurogenesis and neural stem cells in temporal lobe epilepsy

Epilepsy Behav

(2009)

M. Landgrebe et al.

Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas

Neuroimage

(2009)

M. Müller

Frequency representation in the rat cochlea

Hear Res

(1991)

J. Prickaerts et al.

Learning and adult neurogenesis: survival with or without proliferation?

Neurobiol Learn Mem

(2004)

Y. Sakurai

Coding of auditory temporal and pitch information by hippocampal individual cells and cell assemblies in the rat

Neuroscience

(2002)

R.J. Salvi et al.

Auditory plasticity and hyperactivity following cochlear damage

Hear Res

(2000)

J.S. Snyder et al.

A role for adult neurogenesis in spatial long-term memory

Neuroscience

(2005)

W. Sun et al.

Salicylate increases the gain of the central auditory system

Neuroscience

(2009)

J. Syka et al.

Enhancement of the auditory cortex evoked responses in awake guinea pigs after noise exposure

Hear Res

(1994)

M. Uda et al.

Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat

Brain Res

(2006)

G. Yang et al.

Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats

Hear Res

(2007)

J.B. Aimone et al.

Potential role for adult neurogenesis in the encoding of time in new memories

Nat Neurosci

(2006)

G. Andersson et al.

Regional cerebral blood flow during tinnitus: a PET case study with lidocaine and auditory stimulation

Acta Otolaryngol

(2000)

J. Altman et al.

Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats

J Comp Neurol

(1965)

H.G. Belanger et al.

Cognitive sequelae of blast-related versus other mechanisms of brain trauma

J Int Neuropsychol Soc

(2009)

B.A. Bohne

Growth of cochlear damage with increasing severity of exposure

Trans Am Acad Ophthalmol Otolaryngol

(1977)

J. Brown et al.

Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis

Eur J Neurosci

(2003)

J.P. Brown et al.

Transient expression of doublecortin during adult neurogenesis

J Comp Neurol

(2003)

H.A. Cameron et al.

Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus

J Comp Neurol

(2001)

S. Campbell et al.

The role of the hippocampus in the pathophysiology of major depression

J Psychiatry Neurosci

(2004)

K.M. Cave et al.

Blast injury of the ear: clinical update from the global war on terror

Mil Med

(2007)

I. Cernak et al.

Cognitive deficits following blast injury-induced neurotrauma: possible involvement of nitric oxide

Brain Inj

(2001)

H. Chen et al.

Hippocampal cell proliferation regulation by repeated stress and antidepressants

Neuroreport

(2006)

S. Couillard-Despres et al.

Doublecortin expression levels in adult brain reflect neurogenesis

Eur J Neurosci

(2005)

C.F. Dai et al.

Preliminary Study of the relationship between hearing loss and synapses changes in C57BL/6 mouse hippocampus

Abstr Assoc Res Otolaryngol

(2009)

J. Dietrich et al.

CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo

J Biol

(2006)

D. Ding et al.

Cochlear hair cell densities and inner ear staining techniques

R.A. Dobie et al.

Antidepressant treatment of tinnitus patientsInterim report of a randomized clinical trial

Acta Otolaryngol

(1992)

P.K. Duffner

The long-term effects of chemotherapy on the central nervous system

J Biol

(2006)

D. Ehninger et al.

Neurogenesis in the adult hippocampus

Cell Tissue Res

(2008)

Cited by (148)

Noise-induced hearing loss reduces inhibitory neurotransmitter synthesis in ventral hippocampus and contributes to the social memory deficits of mice
2024, Neuroscience Letters
Despite affecting over 1.5 billion people globally, hearing loss (HL) has been referred to as an “invisible disability”, with noise exposure being a major causative factor. Accumulating evidence suggests that HL can induce cognitive impairment. However, relatively little is known about the effects of noise-induced hearing loss (NIHL) on social memory. This study aimed to further investigate the effect of NIHL on social behaviours in mice. We established a rodent model of NIHL using 4-week-old C57BL/6J mice who experienced narrow noise exposure at 116 dB for 3 h per day over two consecutive days. Hearing ability was subsequently evaluated through auditory brainstem response (ABR) testing, and potential changes in the morphology of cochlear hair cells were assessed using immunofluorescence. The sociability and social memory of the mice were evaluated using the three-chamber social interaction test. Noise exposure resulted in complete and persistent HL in C57BL/6J mice, accompanied by severe loss of cochlear hair cells. More importantly, social memory was impaired in adult NIHL mice, whereas their sociability remained intact, these changes were accompanied by a decrease in the protein levels of the inhibitory neuron marker glutamic acid decarboxylase 67 (GAD67) in the ventral hippocampus. This study is the first to confirm that long-term auditory deprivation from HL induced by noise exposure results in social memory deficits in mice without altering their sociability.
Noise-induced auditory damage affects hippocampus causing memory deficits in a model of early age-related hearing loss
2023, Neurobiology of Disease
Several studies identified noise-induced hearing loss (NIHL) as a risk factor for sensory aging and cognitive decline processes, including neurodegenerative diseases, such as dementia and age-related hearing loss (ARHL). Although the association between noise- and age-induced hearing impairment has been widely documented by epidemiological and experimental studies, the molecular mechanisms underlying this association are not fully understood as it is not known how these risk factors (aging and noise) can interact, affecting memory processes. We recently found that early noise exposure in an established animal model of ARHL (C57BL/6 mice) accelerates the onset of age-related cochlear dysfunctions. Here, we extended our previous data by investigating what happens in central brain structures (auditory cortex and hippocampus), to assess the relationship between hearing and memory impairment and the possible combined effect of noise and sensory aging on the cognitive domain. To this aim, we exposed juvenile C57BL/6 mice of 2 months of age to repeated noise sessions (60 min/day, pure tone of 100 dB SPL, 10 kHz, 10 consecutive days) and we monitored auditory threshold by measuring auditory brainstem responses (ABR), spatial working memory, by using the Y-maze test, and basal synaptic transmission by using ex vivo electrophysiological recordings, at different time points (1, 4 and 7 months after the onset of noise exposure, corresponding to 3, 6 and 9 months of age). We found that hearing loss, along with accelerated presbycusis onset, can induce persistent synaptic alterations in the auditory cortex. This was associated with decreased memory performance and oxidative-inflammatory injury in the hippocampus, the extra-auditory structure involved in memory processes. Collectively, our data confirm the critical relationship between auditory and memory circuits, suggesting that the combined detrimental effect of noise and sensory aging on hearing function can be considered a high-risk factor for both sensory and cognitive degenerative processes, given that early noise exposure accelerates presbycusis phenotype and induces hippocampal-dependent memory dysfunctions.
The hearing hippocampus
2022, Progress in Neurobiology
The hippocampus has a well-established role in spatial and episodic memory but a broader function has been proposed including aspects of perception and relational processing. Neural bases of sound analysis have been described in the pathway to auditory cortex, but wider networks supporting auditory cognition are still being established. We review what is known about the role of the hippocampus in processing auditory information, and how the hippocampus itself is shaped by sound. In examining imaging, recording, and lesion studies in species from rodents to humans, we uncover a hierarchy of hippocampal responses to sound including during passive exposure, active listening, and the learning of associations between sounds and other stimuli. We describe how the hippocampus' connectivity and computational architecture allow it to track and manipulate auditory information – whether in the form of speech, music, or environmental, emotional, or phantom sounds. Functional and structural correlates of auditory experience are also identified. The extent of auditory-hippocampal interactions is consistent with the view that the hippocampus makes broad contributions to perception and cognition, beyond spatial and episodic memory. More deeply understanding these interactions may unlock applications including entraining hippocampal rhythms to support cognition, and intervening in links between hearing loss and dementia.
Cerebral consequences of environmental noise exposure
2022, Environment International
The importance of noise exposure as a major environmental determinant of public health is being increasingly recognized. While in recent years a large body evidence has emerged linking environmental noise exposure mainly to cardiovascular disease, much less is known concerning the adverse health effects of noise on the brain and associated neuropsychiatric outcomes. Despite being a relatively new area of investigation, indeed, mounting research and conclusive evidence demonstrate that exposure to noise, primarily from traffic sources, may affect the central nervous system and brain, thereby contributing to an increased risk of neuropsychiatric disorders such as stroke, dementia and cognitive decline, neurodevelopmental disorders, depression, and anxiety disorder. On a mechanistic level, a significant number of studies suggest the involvement of reactive oxygen species/oxidative stress and inflammatory pathways, among others, to fundamentally drive the adverse brain health effects of noise exposure. This in-depth review on the cerebral consequences of environmental noise exposure aims to contribute to the associated research needs by evaluating current findings from human and animal studies. From a public health perspective, these findings may also help to reinforce efforts promoting adequate mitigation strategies and preventive measures to lower the societal consequences of unhealthy environments.
The effect of choline alphoscerate on non spatial memory and neuronal differentiation in a rat model of dual stress
2022, Brain Research
Choline alphoscerate (α-GPC) is a choline-based compound and acetylcholine precursor commonly found in the brain; it has been known to be effective in treating neuronal injury and increasing the levels of acetylcholine (Ach) and brain-derived neurotrophic factor (BDNF) which in turn enhances memory and cognitive function. This study was designed to establish rat models of dual stress using noise and restraint in order to investigate the effect of α-GPC on cognitive function and neuronal differentiation after dual stress. The rats were randomly divided into four groups as follows: a control group (CG), a control with α-GPC group (CDG), a noise-restraint stress group (NRSG), and a noise-restraint stress with α-GPC group (NRSDG). Experimental groups were exposed to a 110 dB sound pressure level (SPL) white band noise and restraint at the same time for 3 h/day for 7 days. Alpha-GPC (400 mg/kg) was administered orally after stress exposure for 7 days. NRSG showed decreased memory function, increased stress hormone, hearing loss, and neuronal damage of the brain. In the hippocampus of NRSG, significantly increased expression of IL-1β and decreased expression of both choline acetyltransferase (ChAT) and BDNF were observed. On the contrary, NRSDG showed better memory function compared to NRSG, which indicates the neuroprotective effect of α-GPC. In addition, NRSDG showed decreased immune response and increased ChAT and BDNF expression as well as neuroblast expression in the hippocampus, which suggests that α-GPC enhances BDNF expression and protects the activity of immature cells in the hippocampus. To the best of our knowledge, this is the first study to show the protective effect of α-GPC on cognitive dysfunction by promotion of neuronal differentiation in an animal model of stress.
Interactions between the hippocampus and the auditory pathway
2022, Neurobiology of Learning and Memory
Increasing evidence has shown that noise overexposure could lead to impaired hippocampal function. Hippocampal alteration is also observed in several auditory deficits, including hearing loss, and tinnitus. Therefore, the functions of hearing and cognition interact with each other. Here, we summarize the evidence that noise affects the hippocampus from aspects of behavior, neurogenesis, ultrastructure, neurotransmission, other biomarkers, and electrophysiology. We also address hippocampal alterations in auditory disorders, including hearing loss and tinnitus. Based on the current state of the field, we point out several aspects that need further investigation. This review is not only to provide a comprehensive summary of the current state of the field but to emphasize that hearing matters in cognition and pave the way for future research.

View all citing articles on Scopus

View full text

Sensory SystemResearch PaperNoise trauma impairs neurogenesis in the rat hippocampus

Abstract

Section snippets

Animals

Inner ear damage after unilateral noise trauma

Discussion

Conclusion

Acknowledgments

Trends Cogn Sci

Biol Psychiatry

Physiol Behav

Neuroscience

Neuroscience

Hear Res

Biol Psychiatry

Neuroscience

Otolaryngol Head Neck Surg

Hear Res

Trends Cogn Sci

Hear Res

J Psychosom Res

Hear Res

Neurobiol Dis

Acta Histochem

Epilepsy Behav

Neuroimage

Hear Res

Neurobiol Learn Mem

Neuroscience

Hear Res

Neuroscience

Neuroscience

Hear Res

Brain Res

Hear Res

Potential role for adult neurogenesis in the encoding of time in new memories

Nat Neurosci

Regional cerebral blood flow during tinnitus: a PET case study with lidocaine and auditory stimulation

Acta Otolaryngol

Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats

J Comp Neurol

Cognitive sequelae of blast-related versus other mechanisms of brain trauma

J Int Neuropsychol Soc

Growth of cochlear damage with increasing severity of exposure

Trans Am Acad Ophthalmol Otolaryngol

Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis

Eur J Neurosci

Transient expression of doublecortin during adult neurogenesis

J Comp Neurol

Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus

J Comp Neurol

The role of the hippocampus in the pathophysiology of major depression

J Psychiatry Neurosci

Blast injury of the ear: clinical update from the global war on terror

Mil Med

Cognitive deficits following blast injury-induced neurotrauma: possible involvement of nitric oxide

Brain Inj

Hippocampal cell proliferation regulation by repeated stress and antidepressants

Neuroreport

Doublecortin expression levels in adult brain reflect neurogenesis

Eur J Neurosci

Preliminary Study of the relationship between hearing loss and synapses changes in C57BL/6 mouse hippocampus

Abstr Assoc Res Otolaryngol

CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo

J Biol

Cochlear hair cell densities and inner ear staining techniques

Antidepressant treatment of tinnitus patientsInterim report of a randomized clinical trial

Acta Otolaryngol

The long-term effects of chemotherapy on the central nervous system

J Biol

Neurogenesis in the adult hippocampus

Cell Tissue Res

Sensory System
Research Paper
Noise trauma impairs neurogenesis in the rat hippocampus