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PLoS One. 2012; 7(6): e39807.
Published online 2012 Jun 29. doi:  10.1371/journal.pone.0039807
PMCID: PMC3387207
PMID: 22768129
Chronic Exposure to Low Frequency Noise at Moderate Levels Causes Impaired Balance in Mice
Haruka Tamura, 1 Nobutaka Ohgami, 1 Ichiro Yajima, 1 Machiko Iida, 1 Kyoko Ohgami, 1 Noriko Fujii, 2 Hiroyuki Itabe, 3 Tastuya Kusudo, 4 Hitoshi Yamashita, 4 and Masashi Kato 1 , *
Georges Chapouthier, Editor

Abstract
We are routinely exposed to low frequency noise (LFN; below 0.5 kHz) at moderate levels of 60–70 dB sound pressure level (SPL) generated from various sources in occupational and daily environments. LFN has been reported to affect balance in humans. However, there is limited information about the influence of chronic exposure to LFN at moderate levels for balance. In this study, we investigated whether chronic exposure to LFN at a moderate level of 70 dB SPL affects the vestibule, which is one of the organs responsible for balance in mice. Wild-type ICR mice were exposed for 1 month to LFN (0.1 kHz) and high frequency noise (HFN; 16 kHz) at 70 dB SPL at a distance of approximately 10–20 cm. Behavior analyses including rotarod, beam-crossing and footprint analyses showed impairments of balance in LFN-exposed mice but not in non-exposed mice or HFN-exposed mice. Immunohistochemical analysis showed a decreased number of vestibular hair cells and increased levels of oxidative stress in LFN-exposed mice compared to those in non-exposed mice. Our results suggest that chronic exposure to LFN at moderate levels causes impaired balance involving morphological impairments of the vestibule with enhanced levels of oxidative stress. Thus, the results of this study indicate the importance of considering the risk of chronic exposure to LFN at a moderate level for imbalance.
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Introduction

Exposure to noise generated in occupational and daily environments is one of the community hazards in our society [1], [2]. Noise consists of sound with broad frequencies, but there is limited information about the frequency-dependent influence of noise on health. Low frequency noise (LFN) is constantly generated from natural and artificial sources. The frequency range of LFN is usually defined as being below 100 Hz, while that of infrasound is usually below 20 Hz [3]. LFN is ubiquitously detected in our modern society and is generated from many occupational and daily sources including transportation systems, industrial devices, air movement devices (e.g., wind turbines, compressors, ventilation and air-conditioning units) and household appliances (e.g., washing machines, refrigerators and freezers). Thus, we are routinely exposed to LFN generated from various devices in the daily environment. In fact, our measurements showed LFN at moderate levels of about 70 dB sound pressure level (SPL) generated from various ordinary devices (Table 1).

Table 1
Typical low frequency noise levels of electric devices in experimental rooms.
Electric devices
Noise levels (dB SPL) at 100 Hz
4°C freezers
65.3±4.8
−30°C freezers
66.1±4.5
−80°C freezers
69.9±2.9
Ice makers
61.8±1.0
Draft chambers
75.5±0.7
Noise levels (means ± SD) were measured by a noise level meter and calculated as an average of five repeated measurements. Noise levels were measured at a distance of approximately 20 cm from the devices shown in Table 1. Background level (mean ± SD) of low frequency noise at 100 Hz was 35.7±2.7 dB SPL in 5 experimental rooms without noise-generating devices shown in Table 1.
Previous studies have indicated that LFN at below 0.5 kHz can be an environmental factor threatening health [4]. In humans, effects of LFN on several physiological functions including the cardiovascular and nervous systems, visual system, auditory system and the endocrine system have been shown [3]. Effects of LFN on the central nervous system including annoyance, sleep and wakefulness, perception, evoked potentials, electroencephalographic changes and cognition have also been shown [5], [6]. Chronic exposure to environmental infrasound has been shown to affect blood pressure, resulting in hypertension in humans [7]. Furthermore, exposure to moderate levels of LFN (70 dB SPL) at the frequency region of 31.5 Hz to 125 Hz for 2 hours has been shown to affect neuroendocrine activity in humans [8]. On the other hand, audible frequencies for humans and mice are known to be approximately 0.02–20 kHz and 1–40 kHz, respectively [9]. Therefore, it is basically difficult for people and mice even without hearing loss to recognize LFN in a noisy environment [3]. Thus, it is important to further analyze the potential risk of occupational and daily exposure to LFN at moderate levels on our health, even if we hardly recognize LFN in daily or occupational environments.

Balance is coordinately regulated by several organs including the vestibule, skeletal muscle and cerebellum [10]. A previous study showed that aging, injuries and other genetic factors can cause abnormal physiological functions in these crucial organs that result in impairments of balance in mice and humans [11], which have a negative impact on quality of life in an aging society. On the other hand, exposure to infrasound (5 Hz and 16 Hz, 95 dB, 5 minutes) has been shown to affect the control of upright standing posture in humans [12]. Also, occupational exposure to LFN has been shown to lead to impairments of vestibular functions [13]. Thus, these previous studies suggest that exposure to LFN can affect balance regulated by vestibular functions in humans. In previous studies with experimental animals, behavior analyses including rotarod, beam-crossing and footprint tests have been used to determine balance [14]–[16]. However, there is very limited information about how chronic exposure to LFN affects balance in mice.

Inner ears contain the vestibule in the vicinity of the organ of Corti. Vestibular hair cells covered with otoconia play an important role in mechanotransduction, by which gravity impulses are converted into neural impulses. Impairments of vestibular hair cells have been shown to cause abnormal behaviors including balance [16]. Thus, the vestibule containing hair cells and an otolith is one of the organs responsible for balance. On the other hand, exposure to a broadband noise (at 1–20 kHz) has been shown to induce ototoxic damage of hair cells with enhanced oxidative stress in the organ of Corti in the inner ear, resulting in noise-induced hearing loss in rodent animal models and humans [17]. In addition, exposure to broadband noise has been shown to enhance oxidative stress in the brain [18], [19]. Thus, it is possible that exposure to noise causes damage of hair cells with increased oxidative stress in inner ears, although those previous studies used broadband noise without consideration of specific frequencies. At present, however, there is no information about whether exposure to LFN enhances oxidative stress in vestibular hair cells, which play a crucial role in regulation of balance.