Aircraft noise exposure affects rat behavior, plasma norepinephrine levels, and cell morphology of the temporal lobe

Aircraft noise exposure affects rat behavior, plasma norepinephrine levels, and cell morphology of the temporal lobe first-author †E-mail:dgq@zju.edu.cn †E-mail:dgq@zju.edu.cn dgq@zju.edu.cn Institute for Environmental Pollution Control Technology, Zhejiang University, Hangzhou 310058, China Institute for Environmental Pollution Control Technology, Zhejiang University, Hangzhou 310058, China In order to investigate the physiological effects of airport noise exposure on organisms, in this study, we exposed Sprague-Dawley rats in soundproof chambers to previously recorded aircraft-related noise for 65 d. For comparison, we also used unexposed control rats. Noise was arranged according to aircraft flight schedules and was adjusted to its weighted equivalent continuous perceived noise levels ( L WECPN ) of 75 and 80 dB for the two experimental groups. We examined rat behaviors through an open field test and measured the concentrations of plasma norepinephrine (NE) by high performance liquid chromatography-fluorimetric detection (HPLC-FLD). We also examined the morphologies of neurons and synapses in the temporal lobe by transmission electron microscopy (TEM). Our results showed that rats exposed to airport noise of 80 dB had significantly lower line crossing number ( P < 0.05) and significantly longer center area duration ( P < 0.05) than control animals. After 29 d of airport noise exposure, the concentration of plasma NE of exposed rats was significantly higher than that of the control group ( P < 0.05). We also determined that the neuron and synapsis of the temporal lobe of rats showed signs of damage after aircraft noise of 80 dB exposure for 65 d. In conclusion, exposing rats to long-term aircraft noise affects their behaviors, plasma NE levels, and cell morphology of the temporal lobe. Aircraft noise Open field test Norepinephrine Neuron Synapse Introduction 1 Studies have shown that aircraft noise has a great impact on the health status of populations residing in areas near air traffic, particularly citing cardiovascular diseases and the use of sleep and cardiovascular medications (Franssen et al., 2004 2004 ; Jarup et al., 2008 2008 ). In addition, researchers have concluded that there is a dose-response relationship between aircraft noise levels and blood pressure of the residents of an area near a military aircraft center (Matsui et al., 2004 2004 ). However, most knowledge of the physiological effects of noise is generally obtained through animal experiment. To begin with, the open field test (OFT) is commonly used as a mechanism to assess the neurobehavioral effects of noise. Katz et al. ( 1981 1981 ) showed that white noise of 95 dB increased motor behaviors of rats in OFT and decreased their defecation after 1 h of acute stress. Food intake in OFT is reduced when rats are exposed to white noise of 95 dB, while their defecation increases (Krebs et al., 1996 1996 ). In addition, the levels of neurotransmitters or hormones in plasma or brain may reflect the neurobiological effects of noise. Typically, the concentrations of norepinephrine (NE) in the brain (Okada et al., 1983 1983 ) and cochlea (Vicente-Torres and Gil-Loyzaga, 1999 1999 ) of rats decrease after acute noise stress. Corticosterone levels in mice plasma have been shown to be significantly increased when exposed to acute noise for 10 min (Vitale et al., 2005 2005 ). Male rats exposed to broadband white noise of 100 dB have been shown to have a significantly increased level of NE in the brain and corticosterone in plasma (Samson et al., 2007 2007 ). Furthermore, observing the morphological changes in neuronal cells can assess the effects of noise. Outer hair cell apoptosis has been observed in the cochlea of chinchilla after intense impulse noise exposure (Hu et al., 2002 2002 ). In addition, continuous noise stress has been shown to affect both degeneration of epithelial cells and apoptosis of stromal cells in the brain of pig (Akdogan et al., 2009 2009 ). We have not found any studies indicating that noise exposure induces morphological damage in the temporal lobe, the lobe related to perception and memory (Suzuki and Baxter, 2009 2009 ). None of the aforementioned studies studied airport noise. Broadband white noise was diffusely applied in previous experimental studies to examine the physiological effects of noise. However, it is important to note that white noise in normal environment is almost non-existent. In China, the aircraft-related weighted equivalent continuous perceived noise level ( L WECPN ) in many residential areas around airports overstepped the 75 dB limit stipulated by the “Standard of Aircraft Noise for Environment around Airport” policy. In this study, we thus sampled actual aircraft noise and played it back to laboratory rats. We then systematically studied their behaviors, plasma NE levels, and cell morphology of the temporal lobe. Materials and methods 1 When airplanes took off at Xiaoshan International Airport (Hangzhou, China), the related noise was recorded using an LDS four-channel dynamic signal analyzer (Photon II, Royston, England), which was stationed on the roof of a nearby residential building (about 100 m vertical distance from the runway). According to the aircrafts’ 24-h flight schedule and airplane type sampled, the intensity of noise was adjusted by a power amplifier (Nor280, Norsonic, Lierskogen, Norway) and played through a dodecahedron non-directional sound source (Nor270, Norsonic, Lierskogen, Norway). The sound absorber and insulation device were optimally assembled so that the L WECPN values of the experimental groups I (EG-I) and II (EG-II) were (75±1.0) dB (equivalent continuous A-weighted sound pressure level ( L Aeq )=65.3 dB) and (80±1.0) dB ( L Aeq =70.3 dB), respectively. In addition, the laboratory was customized to better control acoustics, as the doors were sound-proofed, and the vents were installed with mufflers so that background noise was no more than 40 dBA, the highest sound intensity heard by our control group (CG). We measured the intensity of noise exposure with a sound level meter (AWA6291, Hangzhou, China), which was sound calibrated by a loudspeaker before measurement. Fifty male Sprague-Dawley rats (six weeks old, weighing (150±20) g) were purchased from the Experimental Animal Center of Zhejiang University, and were randomly divided into three groups: CG ( n =10), EG-I ( n =20), and EG-II ( n =20). Rats were housed five per cage and maintained in temperature-controlled ((21±3) °C) rooms with cycles of 12 h of light and 12 h of dark (light on at 8:00 a.m. daily), and allowed free access to water and food. Rats were marked on their fur with picric acid to distinguish individuals. Prior to the experiments, rats were allowed to adapt to the laboratory environment for three days. After this time, aircraft noises were played daily for the animals in groups EG-I and EG-II, whereas the CG was not exposed. OFT and blood collection for neurotransmitter determination were simultaneously conducted at 17:00 on Days 1, 8, 15, 22, 29, and 36 after initial noise exposure (blood collection excluded on Day 36). For OFT, data were collected on the same rats from each group: CG ( n =5), EG-I ( n =10), and EG-II ( n =10). The remaining rats, with corresponding sample sizes of groups, were used for blood collection studies. For investigating long-term effects of airport noise, after 65 d of continuous (excepting time for OFT/blood collection) noise exposure, four rats each were randomly selected from CG and EG-II, respectively, for additional neuronal morphology studies. Animal breeding and experiments were performed in line with the “Quality Management Approach to Laboratory Animals,” and all efforts were made to minimize the number of animals used and their suffering. The size of open field was 100 cm×100 cm×50 cm, and its bottom divided into 25 grids (20 cm×20 cm) by white lines. We termed the nine girds located in the center of the open field as “center area.” The open field was located in a 2.0 m×2.0 m audiometric cabin and lit by a 15-watt red lamp for background lighting. We handled the rats by the base of their tails, carried them to the center of the open field, and allowed them to explore the apparatus for 5 min. The behaviors of the rats were tracked and recorded by the camera fixed above the apparatus. The behaviors we measured included line crossing number and center area duration. In order to assess neurotransmitters in each group, we sampled venous blood (1.0 ml) from the orbital vein. Blood was transferred into 1.5 ml boil-proof microtubes (Axygen, USA) for 10 min of quiescence, and then centrifuged at 4 000 r/min for 10 min at 4 °C. Next 200 μl of supernatant was extracted from each sample, to which 200 μl of 0.05 g/ml perchloric acid was added, followed by shaking the mixture. Mixtures were left at room temperature for 20 min to fully precipitate the plasma proteins, and centrifuged at 10 000 r/min for 15 min. Finally, supernatants were filtered with 0.45 μm membrane filters, and high performance liquid chromatography-fluorimetric detection (HPLC-FLD) was used to measure the concentration of NE. The instrument parameters used for HPLC-FLD were as follows: column, Agilent Zorbax SB-C 18 column (Agilent, US); mobile phase, methanol-buffer (buffer: 0.07 mol NaH 2 PO 4 , 10 mmol sodium octanesulfonate, pH 3.5). The gradient procedure of the mobile phase was as follows: at 0 min, 10% methanol and 90% buffer; at 5 min, 10% methanol and 90% buffer; at 30 min, 60% methanol and 40% buffer (1.0 ml/min of flow rate, 20 μl of injection volume, 35.0 °C of column temperature, 280 nm of fluorescence excitation wavelength, and 315 nm of emission wavelength). Under these conditions, various substances in plasma were completely separated so that no interference to determination of the targets is experienced. After being exposed to aircraft noise for 65 d, four rats were randomly selected from the CG and EG-II groups (two per group). We then examined the neuronal and synaptic morphologies of the temporal lobe by transmission electron microscopy (TEM). Rats were anesthetized by administration of an overdose of sodium pentobarbital and then perfused with glutaraldehyde transcardially. The temporal lobe was localized by digital brain stereotaxic instrument (ZH-LanXing B/S, Huaibei, China) with a soft-type cranial drill. After perfusion for about 1 h, rats were decapitated and the whole brain was stripped and rapidly fixed in glutaraldehyde. After fixation for 24 h, the temporal lobes were removed, cut into thin slices, and fixed in glutaraldehyde for 3 d. Slices were then washed with phosphate buffered saline (PBS), fixed with 0.01 g/ml osmium tetroxide, stained with 0.02 g/ml aqueous solution of uranyl acetate, dehydrated with different concentrations of alcohol and acetone gradient, penetrated and embedded with embedding medium, aggregated in the oven, and finally cut into ultra-thin slices. These slices were then stained with 0.04 g/ml uranyl acetate and citrate, and observed by TEM (Philips Tecnai 10, the Netherlands). Results 1 All data from OFT and HPLC-FLD are expressed as mean±standard error of the mean (SEM). Differences between means for unpaired samples were tested by one-way analysis of variance (ANOVA) using SPSS Version 16 software. The criterion for significance was P < 0.05. Open field test 2 Line crossing number and center area duration were obtained by three individuals working independently, and their mean values were adopted as the final results of OFT. The line crossing number in OFT is shown in Fig. 1a 1a , with no significant difference between CG and EG-I over the duration of the experiment. Nevertheless, the line crossing number of EG-II after 8 d of airport noise exposure was significantly less than that of CG ( P < 0.05). From Fig. 1a 1a , two conclusions can be drawn: long-term exposure to aircraft noise below L WECPN of 75 dB has no significant impact on the line crossing number of rats, while L WECPN of aircraft noise reaching 80 dB is likely to have an impact on line crossing number in rats. There were ten rats in each of EG-I and EG-II and five rats in CG. Data are expressed as mean±SEM. * P < 0.05, compared with the CG (ANOVA) The result of center area duration in OFT showed that the center area durations of CG and EG-I in OFT are almost unchanged, but the center area duration of EG-II is significantly longer than that of CG ( P < 0.05) after the 8 d of noise exposure (Fig. 1b 1b ). On other days, center area duration among the three groups showed no significant difference ( P > 0.05). Levels of plasma NE 2 Fig. 2 2 shows the relationship between the exposure duration of rats to different intensities of aircraft noise and the average concentration of plasma NE measured. We found that there was no significant difference in NE levels between EG-I and CG over the period of the noise exposure. There were ten rats in each of EG-I and EG-II and five rats in CG. Data are expressed as mean±SEM. * P < 0.05, compared with the CG (ANOVA) Nevertheless, on the 29th day of noise exposure, the levels of plasma NE between CG and EG-II showed significant difference ( P < 0.05). By analyzing these results we found that aircraft noise below L WECPN of 75 dB has no significant impact on the plasma NE of rats. Besides, L WECPN of aircraft noise reaching 80 dB is likely to have a negative effect on NE levels under long-term exposure. Therefore, we have known that the intensity of aircraft noise and the duration of aircraft noise exposure are controlling factors to the level of NE in plasma of rats. Temporal lobe cell morphology 2 We observed the neuronal and synaptic morphologies of the temporal lobes from TEM and the representative pictures are shown in Fig. 3 3 . In our experiments, neuronal and synaptic damages were observed in the temporal lobe of EG-II rats, but no damage was seen in the CG. (a) The nuclei (N) in the neurons of the temporal lobe of the CG were oval and their membrane structure was clear, yet mitochondria (M), rough endoplasmic reticula, and other organelles could be seen in cytoplasm, and their distribution was uniform and morphologically normal; (b) The nuclei (N) of neurons in the temporal lobe of EG-II were irregular-shaped, the nuclear membrane was deep-stained and its structure vague, chromatin accumulated along the edge, and cytoplasm was condensed; (c) The synaptic cleft of the temporal lobe area of the CG was clear, and mitochondria and synaptic vesicles were in the synaptic precursor; (d) The synaptic cleft of the temporal lobe area of the EG-II was vague, their chromatin aggregated, and their synaptic vesicles were unclear Discussion 1 Open field test 2 In our study, line crossing is defined as that rats breach the lattices at the bottom of the open field when they are moving during the test and the number of line crossing reflects animals’ horizontal mobility, exploration, and anxiety (Walsh and Cummins, 1976 1976 ). First and foremost, previous studies have shown that motor behaviors of rats in OFT increased after 1 h of acute stress by white noise of 95 dB (Katz et al., 1981 1981 ). However, in our test, rats of EG-I and EG-II showed no significant difference in line crossing compared with CG after 1 d of noise exposure, which means acute effects of noise exposure were not evident in our experiment. It may be that noise intensity below L WECPN of 80 dB is “moderate” to rats. In addition, after suffering airport noise exposure for 8 d, rats of EG-II showed that the line crossing number decreased, which means horizontal mobility and exploration ability of the rat decreased and some anxiety appeared (Walsh and Cummins, 1976 1976 ). However, Pan et al. ( 2006 2006 ) found that two weeks’ noise stress (2 h/d, 85 dB) increased square crossing and vertical movement, which is in contrast to our results. There are a number of possible explanations. First, the intensity of noise is an important factor. Second, the duration of daily noise exposure cannot be ignored because, in our test aircraft, noise was exposed throughout the day. Third, the neurobehavioral effect of continuous white noise is different from that of intermittent aircraft noise (Hou, 2002 2002 ). Last but not least, from Fig. 1a 1a , we also know that line crossing of rats was not significantly different between CG and EG-II except on the 8th day. The reason is that behaviors of rats manifest itself differently depending on the duration of stress (Silveira et al., 2000 2000 ). Conrad et al. ( 1999 1999 ) have also shown that behaviors of rats turned from an excited state to inhibitory state under prolonged stress. Another reason may be that the mechanisms of resistance and/or adaptability are generated after longer-term noise stress. In our study, center area duration is defined as latency of the rats before leaving the center area, which is measured by anxiety-like behavior. As is known, high center area duration indicates high anxiety levels (Walsh and Cummins, 1976 1976 ). Thus, the emotions of rats in EG-II altered to anxiety after 8 d of noise exposure. The results of center area duration on other days suggest that the effect of aircraft noise on anxiety is not permanent. This conclusion is also in line with the line crossing results. Levels of plasma NE 2 Epinephrine, NE, and cortisol are stress hormones that are used as indicators of body stress upon noise exposure (Vaernes et al., 1982 1982 ; Okada et al., 1983 1983 ; Spreng, 2000 2000 ; Li et al., 2009 2009 ). NE plays an important role as a stress hormone in conducting and adapting to stress (Goldstein, 1981 1981 ; Finlay et al., 1995 1995 ; Murchison et al., 2004 2004 ). Therefore, plasma NE level of EG-II increased after long-term noise exposure (29 d) in our experiment, possibly due to the cumulative effect of high intensity noise. Unfortunately, we do not know the plasma NE level of rats after 29 d of noise exposure, because it is difficult to collect blood from more fierce rats. Plasma NE is primarily secreted by the sympathetic nerve endings of the heart, blood vessels, and adrenal medulla, and is controlled by the sympathetic nervous system (Esler et al., 1990 1990 ). Plasma NE levels reflect the excitability of the peripheral sympathetic system (Lake et al., 1981 1981 ; Raskind et al., 1984 1984 ). Due to aircraft noise exposure in our experiments, the levels of NE in rat plasma increased, indicating that aircraft noise stimulates sympathetic excitement of the adrenal medulla system. Several studies have shown that trait anxiety is significantly associated with increased NE concentration in blood plasma. Individuals with higher plasma NE concentrations also have more severe anxiety symptoms and the concentrations of plasma NE of patients with anxiety disorders are drastically higher than those of healthy individuals (Yasunari et al., 2006 2006 ). We conclude that high intensity aircraft noise exposure may similarly induce anxiety symptoms in rats. Further, patients with hypertension have also been found to have higher plasma NE concentrations (Makino et al., 2006 2006 ). In addition, epidemiological investigations have pointed out that the incidences of heart disease and hypertension are directly related to aircraft noise exposure (Knipschild, 1977 1977 ; Franssen et al., 2004 2004 ). Our results partly provide pathological evidence supporting this epidemiological research. Temporal lobe cell morphology 2 Previous studies have shown that necrosis and apoptosis of neurons occur when the body is subject to physical, chemical, or severe pathological stimulation (Bonfoco et al., 1995 1995 ). For this reason, we consider that the long-term noise stress in rats resulted in the lesions in temporal lobe neurons and synapses of EG-II. In the central nervous system (CNS), the temporal lobe areas are closely related to perception and memory (Baxter, 2009 2009 ). Therefore, when neurons of the temporal lobe are damaged, a variety of mental disorders are likely to occur, such as cognitive decline, memory reduction, or subjective emotional instability (Hugdahl et al., 2009 2009 ). When synaptic morphology changes, the related functions of the brain and CNS change accordingly, further leading to changes in behavior (de Bartolomeis and Fiore, 2004 2004 ). The results of our experiments are consistent with changes in rat behavior due to long-term exposure of aircraft noise. Conclusions 1 In conclusion, exposing rats to long-term aircraft noise affects their behavior, specifically in the form of inhibiting mobility and increasing anxiety. Our data indicate that plasma NE levels of rats increase as a result of aircraft noise exposure. Furthermore, our findings indicate that aircraft noise exposure leads to damages of neuronal and synaptic structures of the temporal lobe in rats. Nevertheless, additional studies are necessary to further investigate the mechanisms involved. References O Akdogan , A Selcuk , G Take , D Erdoğan , H Dere . Continuous or intermittent noise exposure, does it cause vestibular damage? An experimental study . Auris Nasus Larynx , 2009 . 36 ( 1 ): 2 - 6 . 18482810 DOI: 10.1016/j.anl.2008.03.003 http://doi.org/10.1016/j.anl.2008.03.003 . Continuous or intermittent noise exposure, does it cause vestibular damage? 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Anxiety-induced plasma norepinephrine augmentation increases reactive oxygen species formation by monocytes in essential hypertension We sincerely thank Dr. Jian SHI (Department of Neurosurgery, the Second Affiliated Hospital, School of Medicine, Zhejiang University, China) for the help on dissecting the rats, and Dr. Xin-hang JIANG (College of Life Sciences, Zhejiang University, China) for the help on measuring the concentrations of NE in this study. 10.1631/jzus.B1000439 Project supported by the National Natural Science Foundation of China (No. 1060408), and the National Public Benefit Research Foundation of China (No. 200809142) 2010-12-19 2011-11-11 2011-08-29 2022-01-05 Copyright © Zhejiang University and Springer-Verlag Berlin Heidelberg 2011 2011 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 12 12