High-Frequency Hearing Loss Is Associated With Anxiety and Brain Structural Plasticity in Older Adults

Ma, Wen; Zhang, Yue; Li, Xiao; Liu, Siqi; Gao, Yuting; Yang, Jing; Xu, Lixin; Liang, Hudie; Ren, Fuxin; Gao, Fei; Wang, Yao

doi:10.3389/fnagi.2022.821537

Cited by 8 publications

(7 citation statements)

References 37 publications

(50 reference statements)

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“…Anxiety is often followed by hearing disabilities, such as hearing loss or tinnitus, and hearing loss‐related anxiety was examined in another recent study 7 . Acoustic trauma has been shown to affect limbic systems, including the cingulate cortex 77 and hippocampus, 7 and also enhances connectivity between the auditory system, amygdala, and hippocampus, 78–80 resulting in anxiety‐like behaviors. Exposure to loud noise is widely used to experimentally induce hearing loss in laboratory animals 7,81 .…”

Section: Discussionmentioning

confidence: 99%

Microglial activation in the lateral amygdala promotes anxiety‐like behaviors in mice with chronic moderate noise exposure

Peng,

Mao,

Liu

et al. 2024

CNS Neurosci Ther

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BackgroundLong‐term non‐traumatic noise exposure, such as heavy traffic noise, can elicit emotional disorders in humans. However, the underlying neural substrate is still poorly understood.MethodsWe exposed mice to moderate white noise for 28 days to induce anxiety‐like behaviors, measured by open‐field, elevated plus maze, and light–dark box tests. In vivo multi‐electrode recordings in awake mice were used to examine neuronal activity. Chemogenetics were used to silence specific brain regions. Viral tracing, immunofluorescence, and confocal imaging were applied to define the neural circuit and characterize the morphology of microglia.ResultsExposure to moderate noise for 28 days at an 85‐dB sound pressure level resulted in anxiety‐like behaviors in open‐field, elevated plus maze, and light–dark box tests. Viral tracing revealed that fibers projecting from the auditory cortex and auditory thalamus terminate in the lateral amygdala (LA). A noise‐induced increase in spontaneous firing rates of the LA and blockade of noise‐evoked anxiety‐like behaviors by chemogenetic inhibition of LA glutamatergic neurons together confirmed that the LA plays a critical role in noise‐induced anxiety. Noise‐exposed animals were more vulnerable to anxiety induced by acute noise stressors than control mice. In addition to these behavioral abnormalities, ionized calcium‐binding adaptor molecule 1 (Iba‐1)‐positive microglia in the LA underwent corresponding morphological modifications, including reduced process length and branching and increased soma size following noise exposure. Treatment with minocycline to suppress microglia inhibited noise‐associated changes in microglial morphology, neuronal electrophysiological activity, and behavioral changes. Furthermore, microglia‐mediated synaptic phagocytosis favored inhibitory synapses, which can cause an imbalance between excitation and inhibition, leading to anxiety‐like behaviors.ConclusionsOur study identifies LA microglial activation as a critical mediator of noise‐induced anxiety‐like behaviors, leading to neuronal and behavioral changes through selective synapse phagocytosis. Our results highlight the pivotal but previously unrecognized roles of LA microglia in chronic moderate noise‐induced behavioral changes.

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Section: Discussionmentioning

confidence: 99%

Microglial activation in the lateral amygdala promotes anxiety‐like behaviors in mice with chronic moderate noise exposure

Peng,

Mao,

Liu

et al. 2024

CNS Neurosci Ther

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“…Inadequate sleep duration might affect fluid absorption and ion homeostasis and destruct hair cells in the cochlea by inflammatory cytokines and thus impair sensory transduction ( 12 ). Change of hippocampal structure is another potential procedure, by which sleep disturbed neural input from the central auditory system ( 11 , 13 ). Also, sleep curtailment strikingly altered metabolic and endocrine function, causing eustachian tube dysfunction and poorer nerve conduction ( 45 , 46 ).…”

Section: Discussionmentioning

confidence: 99%

“…Sleep architecture changes with growing age in human beings, which are embodied in shorter sleep duration, sleep fragment and poorer sleep quality ( 10 ). It was reported that sleep might affect hearing condition by disrupting fluid absorption and ion homeostasis, destructing hair cells in the cochlea and changing neural input from the central auditory system ( 11 – 13 ). Being considered as a behavior distinct from nocturnal sleep, midday napping is common in both many countries and more prevalent in the old ( 14 – 17 ).…”

Section: Introductionmentioning

confidence: 99%

Association of nocturnal sleep duration and midday napping with subjective poor hearing among middle-aged and older adults in China

Cui

Guo

et al. 2023

Front. Public Health

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BackgroundHearing loss has occurred as a critical concern for aging and health. However, it remains unknown whether nocturnal sleep and midday napping duration are associated with hearing loss in middle-aged and older adults.MethodsThe study comprised 9,573 adults from China Health and Retirement Longitudinal Study, who have completed the survey for sleep characteristics and subjective functional hearing. We collected self-reported nocturnal sleep duration (<5, 5 to <6, 6 to <7, 7 to <9, ≥9 h/night) and midday napping duration (≤5, 5 to ≤30, and >30 min). The sleep information was classified into different sleep patterns. The primary outcome was self-reported hearing loss events. Multivariate Cox regression models and restricted cubic splines were used to investigate the longitudinal association of sleep characteristics with hearing loss. We applied Cox generalized additive models and bivariate exposure-response surface diagrams to visualize the effects of different sleep patterns on hearing loss.ResultsWe confirmed 1,073 cases of hearing loss (55.1% female) during the follow-up. After adjusting for demographic characteristics, lifestyle factors and health condition, nocturnal sleep with < 5 h was positively associated with hearing loss [hazard ratio (HR): 1.45, 95% confidence interval [CI]: 1.20, 1.75]. Individuals with napping for 5 to ≤30 min had a 20% (HR: 0.80, 95%CI: 0.63, 1.00) lower risk of hearing loss compared with those with napping ≤ 5 min. Restrictive cubic splines showed the reverse J-shaped association between nocturnal sleep and hearing loss. Moreover, we found significant joint effects of sleeping < 7 h/night and midday napping ≤ 5 min (HR: 1.27, 95% CI: 1.06, 1.52) on hearing loss. Bivariate exposure-response surface diagrams also reflected the finding that short sleep without napping existed the highest risk of hearing loss. Compared with persistently sleeping moderately (7–9 h/night), those who persistently slept < 7 h/night or shifted from < 7 h/night to moderate or > 9 h/night had higher risks of hearing loss.ConclusionInadequate nocturnal sleep was associated with an elevated risk of poor subjective hearing in middle-aged and older adults, while moderate napping decreased the risk of hearing loss. Keeping sleep stable within recommendation duration may be a useful strategy for preventing poor hearing loss.

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“…Additional studies ( Chern et al, 2022 ; Huang et al, 2022 ) have suggested that HL can contribute to psychosocial disorders in patients. An MRI study revealed that gray matter volume in the middle cingulate cortex is positively correlated with high-frequency hearing impairment in patients with ARHL ( Ma et al, 2022 ). These results suggest that HL can influence mental health.…”

Section: Sensory Deprivation Hypothesismentioning

confidence: 99%

Sensorineural hearing loss and cognitive impairment: three hypotheses

Zhao,

Wang,

Cui

et al. 2024

Front. Aging Neurosci.

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Sensorineural hearing loss (SNHL) is a category of hearing loss that often leads to difficulty in understanding speech and other sounds. Auditory system dysfunction, including deafness and auditory trauma, results in cognitive deficits via neuroplasticity. Cognitive impairment (CI) refers to an abnormality in the brain’s higher intellectual processes related to learning, memory, thinking and judgment that can lead to severe learning and memory deficits. Studies have established a strong correlation between SNHL and CI, but it remains unclear how SNHL contributes to CI. The purpose of this article is to describe three hypotheses regarding this relationship, the mainstream cognitive load hypothesis, the co-morbidity hypothesis, and the sensory deprivation hypothesis, as well as the latest research progress related to each hypothesis.

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High-Frequency Hearing Loss Is Associated With Anxiety and Brain Structural Plasticity in Older Adults

Cited by 8 publications

References 37 publications

Microglial activation in the lateral amygdala promotes anxiety‐like behaviors in mice with chronic moderate noise exposure

Microglial activation in the lateral amygdala promotes anxiety‐like behaviors in mice with chronic moderate noise exposure

Association of nocturnal sleep duration and midday napping with subjective poor hearing among middle-aged and older adults in China

Sensorineural hearing loss and cognitive impairment: three hypotheses

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