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Selective Degeneration of Synapses in the Dorsal Cochlear Nucleus of Chinchilla Following Acoustic Trauma and Effects of Antioxidant Treatment

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Selective Degeneration of Synapses in the Dorsal Cochlear Nucleus of Chinchilla Following Acoustic Trauma and Effects of Antioxidant Treatment Hearing Research 283 (2012) 1e13 Contents lists available at SciVerse ScienceDirect Hearing Research journal homepage: www.elsevier.com/locate/heares Research paper Selective degeneration of synapses in the dorsal cochlear nucleus of chinchilla following acoustic trauma and effects of antioxidant treatment Xiaoping Du a, Kejian Chen a,1, Chul-Hee Choi a,2, Wei Li a, Weihua Cheng a, Charles Stewart a,b, Ning Hu a, Robert A. Floyd b, Richard D. Kopke a,c,d,* a Hough Ear Institute, Oklahoma, OK 73112, USA b Experimental Therapeutic Research Program, Oklahoma Medical Research Foundation, Oklahoma, OK 73104, USA c Department of Physiology, University of Oklahoma Health Sciences Center, Oklahoma, OK 73104, USA d Department of Otolaryngology, University of Oklahoma Health Sciences Center, Oklahoma, OK 73104, USA article info abstract Article history: The purpose of this study was to reveal synaptic plasticity within the dorsal cochlear nucleus (DCN) as Received 31 May 2011 a result of noise trauma and to determine whether effective antioxidant protection to the cochlea can Received in revised form also impact plasticity changes in the DCN. Expression of synapse activity markers (synaptophysin and 18 November 2011 precerebellin) and ultrastructure of synapses were examined in the DCN of chinchilla 10 days after Accepted 30 November 2011 a 105 dB SPL octave-band noise (centered at 4 kHz, 6 h) exposure. One group of chinchilla was treated Available online 9 December 2011 with a combination of antioxidants (4-hydroxy phenyl N-tert-butylnitrone, N-acetyl-L-cysteine and acetyl-L-carnitine) beginning 4 h after noise exposure. Down-regulated synaptophysin and precerebellin expression, as well as selective degeneration of nerve terminals surrounding cartwheel cells and their primary dendrites were found in the fusiform soma layer in the middle region of the DCN of the noise exposure group. Antioxidant treatment significantly reduced synaptic plasticity changes surrounding cartwheel cells. Results of this study provide further evidence of acoustic trauma-induced neural plas- ticity in the DCN and suggest that loss of input to cartwheel cells may be an important factor contributing to the emergence of hyperactivity in the DCN after noise exposure. Results further suggest that early antioxidant treatment for acoustic trauma not only rescues cochlear hair cells, but also has impact on central auditory structures. Ó 2011 Elsevier B.V. All rights reserved. 1. Introduction 2002; Heffner and Harrington, 2002; House and Brackmann, 1981; Kaltenbach, 2006; Pulec, 1995; Sziklai, 2004). Among the Acoustic trauma is the leading cause of hearing loss and tinnitus hypotheses for a central origin of tinnitus, many studies have both in the military and in the civilian population (Nelson et al., focused on the dorsal cochlear nucleus (DCN). For example, elec- 2005; Saunders and Griest, 2009). Noise-induced hearing loss is trophysiological studies have demonstrated hyperactivity in the mainly caused by hair cell damage/death through mechanical and DCN after noise exposure (Kaltenbach et al., 2005; Kaltenbach, metabolic mechanisms (Le Prell et al., 2007; Slepecky, 1986; 2006). Animals with psychophysical evidence of noise-induced Yamane et al., 1995a, b). The mechanisms of noise-induced tinnitus had elevated spontaneous activity in the DCN, suggesting tinnitus, however, are less clear. There have been many hypoth- that such hyperactivity may be related to noise-induced tinnitus eses, some focused on the auditory periphery while others (Brozoski et al., 2002; Kaltenbach et al., 2004). The same dose of emphasize the importance of changes in the CNS (Brozoski et al., noise exposure that causes hyperactivity in the DCN also causes tinnitus in animals (Heffner and Harrington, 2002). Furthermore, up-regulation of cholinergic and glutamate receptors, elevated * Corresponding author. Hough Ear Institute, P.O. Box 23206, Oklahoma, OK glutamatergic synaptic release, and depressed glutamate uptake 73123, USA. Tel.: þ1 405 639 2876; fax: þ1 405 947 6226. have been observed in both the ventral cochlear nucleus (VCN) and E-mail address: [email protected] (R.D. Kopke). DCN after noise exposure (Kaltenbach and Zhang, 2007; Muly et al., 1 Present address: Spatial Orientation Center, Naval Medical Center, San Diego, 2004). Weeks after noise exposure, expression of a glycine receptor CA, USA. a 2 Present address: Audiology & Speech-Language Pathology, College of Medical subunit (GlyR 1) decreased in the fusiform soma layer (FSL) at the Sciences, Catholic Univ. of Daegu, Kyungsansi, South Korea. middle and high frequency regions of the DCN (Wang et al., 2009). 0378-5955/$ e see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.heares.2011.11.013 2 X. Du et al. / Hearing Research 283 (2012) 1e13 These results suggest an excitotoxicity mechanism in the DCN after 2. Materials and methods noise exposure. In the excitotoxicity mechanism, toxic concentra- tions of glutamate or imbalance of excitatory and inhibitory amino 2.1. Animals, noise exposure and antioxidant injection acids will lead to osmotic imbalance across the post-synaptic membrane, and result in fluid entry into cells, swelling of cells, All tissue samples used in this study were collected from our rupturing of cell membranes and degeneration (Le Prell et al., previous study except tissue samples for TEM study. Noise expo- 2007). sure, administration of antioxidants and measurement of auditory Pathological changes have been found in the central auditory brainstem responses were detailed in our previous reports (Choi system, especially in the cochlear nucleus (CN), after noise expo- et al., 2008; Du et al., 2011). In brief, the chinchilla were random- sure (Aarnisalo et al., 2000; Basta et al., 2005; Gröschel et al., 2010; ized into 3 groups (n ¼ 7 in each group, 6 for histology and 1 for Kim et al., 1997, 2004a,b,c; Morest et al., 1998; Muly et al., 2004; TEM study): Animals in the noise exposure plus carrier solution Theopold, 1975). The number or density of axons in the chinchilla (dimethyl sulfoxide, polyethylene glycol 400, and saline) and noise posterior ventral cochlear nucleus (PVCN) was decreased by about plus treatment (noise/treatment) groups were exposed to a 105 dB half (Bilak et al., 1997). However, the number of inhibitory endings sound pressure level (SPL) octave-band noise (OBN) for 6 h. only partially recovered while excitatory synapses were fully Animals in the normal control group were not exposed to noise. An restored by 24e32 weeks (Kim et al., 2004a). Excitatory terminals initial antioxidant injection was given to animals in the noise/ displayed progressive increases in neurofilaments and enlarged treatment group 4 h after noise exposure and then twice a day for synaptic vesicles in the PVCN weeks after noise exposure. Inhibi- the following 2 days. Animals in this group received 20 mg/kg of tory terminals darkened while some vesicles disintegrated and 4-HOPBN dissolved in dimethyl sulfoxide (40%), polyethylene many smaller flatter vesicles collapsed (Kim et al., 2004b, c). glycol 400 (40%), and saline (20%), 50 mg/kg of 20% NAC in water Degeneration of synapsing nerve endings of secondary neurons (containing 0.05% edetate disodium, dehydrate, PH 7.0, Hospira Inc., was found in the anterior ventral cochlear nucleus (AVCN) and lake Forest, IL), and 20 mg/kg of ALCAR (SigmaeAldrich Inc. St. octopus cell area of the PVCN (Theopold, 1975). These areas receive Louis, MO) in saline. These agents were intraperitoneally admin- afferent input from the cochlea. Reduction of neuropil volume and istered separately. Equal volumes of carrier solution were injected neuron size, and increases in neuronal packing density with into animals in the noise exposure and the normal control groups at minimal changes in neuron number were observed in the VCN and the same time points as in the noise/treatment group. ABR deep layer (DL) of the DCN, but not in layers 1 and 2 of the DCN that thresholds for both ears of each animal were measured before noise have no direct input from the cochlea (Willott et al., 1994). exposure (baseline), immediately after, and then 10 days after noise However, nerve terminals in the DCN have not been well examined exposure (Choi et al., 2008). in noise exposed animals. For noise exposure, two chinchilla at a time were placed in two In the DCN, fusiform and giant cells are the projecting cells and small wire restraint cages on a wooden plate in a sound isolation receive direct auditory nerve inputs. Cartwheel cells, major booth (Industrial Acoustics Company, New York, NY) and exposed inhibitory inter-neurons, receive synaptic inputs from the granule to 105 dB SPL OBN centered at 4 kHz for 6 h. The noise was cell-parallel fiber system and send their axons to form synapses on generated, filtered by a Tucker Davis Technologies device (TDT, fusiform cells, giant cells and also on other cartwheel cells (Davis Alachua, FL), amplified by an audio power amplifier (QSC PLX 3402, and Young, 1997; Golding and Oertel, 1996, 1997; Wouterlood Costa Mesa, CA), and transduced with an acoustic speaker and Mugnaini, 1984). Granule cells in the DCN receive (JBL 2350, Northridge, CA). The speaker was positioned directly converging inputs from both auditory and non-auditory systems above the wire cages. During noise exposure, a condenser micro- (Burian and Gestoettner, 1988; Itoh et al., 1987; Weedman et al., phone (B&K 2804, Norcross, GA) was used to continually monitor 1996). Evidence supporting the DCN’s role in tinnitus generation the noise level. has been reviewed by Kaltenbach and Godfrey (2008). Although studies suggested that the hyperactivity recorded in the DCN may 2.2. Cochlear and brain tissue processing and hair cell counting be from fusiform cells (Brozoski et al., 2002; Finlayson and Kaltenbach, 2009), some studies have suggested that cartwheel After the last ABR measurement, 18 chinchilla (6 in each group) cells may be involved (Chang et al., 2002; Kaltenbach and Zhang, were euthanized with an overdose of ketamine and xylazine, and 2007).
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