Changes in the immunohistochemical localization of the glycine receptor in the superior olivary complex of adult circling mice

Yoo,Young‑Bok; Maskey,Dhiraj; Kim,Myeung Ju

doi:10.3892/mmr.2015.4431

Changes in the immunohistochemical localization of the glycine receptor in the superior olivary complex of adult circling mice

Authors:
- Young‑Bok Yoo
- Dhiraj Maskey
- Myeung Ju Kim
View Affiliations

Affiliations: Department of Anatomy, Dankook University, College of Medicine, Cheonan‑si, South Chungcheong 330‑714, Republic of Korea, Department of Anatomy, Nepalese Army Institute of Health Sciences‑College of Medicine, Sanobharyang, Kathmandu 10160, Nepal
Published online on: October 13, 2015 https://doi.org/10.3892/mmr.2015.4431
Pages: 7927-7932
Copyright: © Yoo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Circling mice is a mutant model of spontaneous deafness exhibiting degenerated spiral ganglion cells in the cochlea and loss of organ of Corti. The balance between glycinergic inhibition and glutamatergic excitation in the lateral superior olive (LSO) is essential for the detection of interaural level differences. Long term weakening of glycinergic synaptic inhibition in the LSO may lead to the downregulation of synaptic release of glycine in dorsal cochlear nucleus and downregulation of postsynaptic glycine receptor (GlyR) activity in the LSO, which may contribute to hearing loss. The present study utilized an immunohistochemical method to assess changes in GlyR immunoreactivity (IR) and the cell number in the superior olivary complex (SOC) of heterozygote (+/cir) and homozygote (cir/cir) circling mice. A significant decrease in the IR was observed in all nuclei of the SOC of homozygous mice. Loss of GlyR immunoreactive cells and a decrement in cell size was also observed in the homozygotes. A decrease in the GlyR IR in the neurons and neuropils, cell number and size of the cir/cir, may lead to profound changes in inhibitory transmission and the functional properties in the SOC nuclei. Therefore, the functional loss of inhibitory neurotransmitters in the brainstem may result in deafness of adult cir/cir mice.

View Figures

View References

1	Lee JW, Lee EJ, Hong SH, Chung WH, Lee HT, Lee TW, Lee JR, Kim HT, Suh JG, Kim TY and Ryoo ZY: Circling mouse: Possible animal model for deafness. Comp Med. 51:550–554. 2001.
2	Syka J: Plastic changes in the central auditory system after hearing loss, restoration of function and during learning. Physiol Rev. 82:601–636. 2002. View Article : Google Scholar : PubMed/NCBI
3	Potashner SJ, Suneja SK and Benson CG: Regulation of D-aspartate release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp Neurol. 148:222–235. 1997. View Article : Google Scholar : PubMed/NCBI
4	Potashner SJ, Suneja SK and Benson CG: Altered glycinergic synaptic activities in guinea pig brain stem auditory nuclei after unilateral cochlear ablation. Hear Res. 147:125–136. 2000. View Article : Google Scholar : PubMed/NCBI
5	Milbrandt JC, Hunter C and Caspary DM: Alterations of GABAA receptor subunit mRNA levels in the aging Fischer 344 rat inferior colliculus. J Comp Neurol. 379:455–465. 1997. View Article : Google Scholar : PubMed/NCBI
6	Nakagawa H, Sato K, Shiraishi Y, Kuriyama H and Altschuler RA: NMDAR1 isoforms in the rat superior olivary complex and changes after unilateral cochlear ablation. Brain Res Mol Brain Res. 77:246–257. 2000. View Article : Google Scholar : PubMed/NCBI
7	Von Hehn CA, Bhattacharjee A and Kaczmarek LK: Loss of Kv3.1 tonotopicity and alterations in cAMP response element-binding protein signaling in central auditory neurons of hearing impaired mice. J Neurosci. 24:1936–1940. 2004. View Article : Google Scholar : PubMed/NCBI
8	Garcia MM, Edward R, Brennan GB and Harlan RE: Deafferentation induced changes in protein kinase C expression in the rat cochlear nucleus. Hear Res. 147:113–124. 2000. View Article : Google Scholar : PubMed/NCBI
9	Idrizbegovic E, Bogdanovic N and Canlon B: Modulating calbindin and parvalbumin immunoreactivity in the cochlear nucleus by moderate noise exposure in mice. A quantitative study on the dorsal and posteroventral cochlear nucleus. Brain Res. 800:86–96. 1998. View Article : Google Scholar : PubMed/NCBI
10	Suneja SK and Potashner SJ: ERK and SAPK signaling in auditory brainstem neurons after unilateral cochlear ablation. J Neurosci Res. 73:235–245. 2003. View Article : Google Scholar : PubMed/NCBI
11	Bledsoe SC Jr, Nagase S, Miller JM and Altschuler RA: Deafness induced plasticity in the mature central auditory system. Neuroreport. 7:225–229. 1995. View Article : Google Scholar : PubMed/NCBI
12	Nagase S, Miller JM, Dupont J, Lim HH, Sato K and Altschuler RA: Changes in cochlear electrical stimulation induced Fos expression in the rat inferior colliculus following deafness. Hear Res. 147:242–250. 2000. View Article : Google Scholar : PubMed/NCBI
13	Legendre P: The glycinergic inhibitory synapse. Cell Mol Life Sci. 58:760–793. 2001. View Article : Google Scholar : PubMed/NCBI
14	Caspery DM: Electrophysiological studies of glycinergic mechanisms in auditory brainstem structures. Ottersen OP and Storm-Mathisen J: Glycine Neurotransmission Chichester: Wiley; pp. 453–483. 1990
15	Wenthold RJ, Huie D, Altschuler RA and Reeks KA: Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience. 22:897–912. 1987. View Article : Google Scholar : PubMed/NCBI
16	Wenthold RJ and Hunter C: Immunocytochemistry of glycine and glycine receptors in the central auditory system. Ottersen OP and Storm-Mathisen J: Glycine Neurotransmission, Chichester: Wiley; pp. 391–416. 1990
17	Vater M, Habbicht H, Kössl M and Grothe B: The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats. J Comp Physiol A. 171:541–553. 1992. View Article : Google Scholar : PubMed/NCBI
18	Kavanagh GL and Kelly JB: Midline and lateral feld sound localization in the ferret (MustelaPutorius): Contribution of the superior olivary complex. J Neurophysiol. 67:1643–1658. 1992.PubMed/NCBI
19	O'Neill WE, Zettel ML, Whittemore KR and Frisina RD: Calbindin D-28k immunoreactivity in the medial nucleus of the trapezoid body declines with age in C57BL/6, but not CBA/CaJ, mice. Hear Res. 112:158–166. 1997. View Article : Google Scholar : PubMed/NCBI
20	Banks MI and Smith PH: Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci. 12:2819–2837. 1992.PubMed/NCBI
21	Suneja SK, Benson CG and Potashner SJ: Glycine receptors in adult guinea pig brain stem auditory nuclei: Regulation after unilateral cochlear ablation. Exp Neurol. 154:473–488. 1998. View Article : Google Scholar
22	Suneja SK, Potashner SJ and Benson CG: Plastic changes in glycine and GABA release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp Neurol. 151:273–288. 1998. View Article : Google Scholar : PubMed/NCBI
23	Willott JF and Turner JG: Neural plasticity in the mouse inferior colliculus: Relationship to hearing loss, augmented acoustic stimulation and prepulse inhibition. Hear Res. 147:275–281. 2000. View Article : Google Scholar : PubMed/NCBI
24	Krenning J, Hughes LF, Caspary DM and Helfert RH: Age-related glycine receptor subunit changes in the cochlear nucleus of Fischer-344 rats. Laryngoscope. 108:26–31. 1998. View Article : Google Scholar : PubMed/NCBI
25	Buras ED, Holt AG, Griffith RD, Asako M and Altschuler RA: Changes in glycine immunoreactivity in the rat superior olivary complex following deafness. J Comp Neurol. 494:179–189. 2006. View Article : Google Scholar
26	Kandler K and Friauf E: Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci. 15:6890–6904. 1995.PubMed/NCBI
27	Gillespie DC, Kim G and Kandler K: Inhibitory synapses in the developing auditory system are glutamatergic. Nat Neurosci. 8:332–338. 2005. View Article : Google Scholar : PubMed/NCBI
28	Hong SH, Kim MJ and Ahn SC: Glutamatergic transmission is sustained at a later period of development of medial nucleus of the trapezoid body-lateral superior olive synapses in circling mice. J Neurosci. 28:13003–13007. 2008. View Article : Google Scholar : PubMed/NCBI
29	Schwartz IR: The superior olivary complex and lateral lemniscal nuclei. Webster B, Popper AN and Fay RR: The Mammalian Auditory Pathways: Neuroanatomy New York: Springer; pp. 117–167. 1990
30	Friauf E, Hammerschmidt B and Kirsch J: Development of adult-type inhibitory glycine receptors in the central auditory system of rats. J Comp Neurol. 385:117–134. 1997. View Article : Google Scholar : PubMed/NCBI
31	Maskey D, Kim M, Aryal B, Pradhan J, Choi IY, Park KS, Son T, Hong SY, Kim SB, Kim HG and Kim MJ: Effect of 835 MHz radio-frequency radiation exposure on calcium binding proteins in the hippocampus of the mouse brain. Brain Res. 1313:232–241. 2010. View Article : Google Scholar
32	Paxinos G and Franklin KBJ: The Mouse Brain in Stereotaxic Coordinates. Second edition: San Diego: Academic Press; 2001
33	Sanes DH and Friauf E: Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res. 147:46–58. 2000. View Article : Google Scholar : PubMed/NCBI
34	Kapfer C, Seidl AH, Schweizer H and Grothe B: Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat Neurosci. 5:247–253. 2002. View Article : Google Scholar : PubMed/NCBI
35	Kim J, Morest DK and Bohne BA: Degeneration of axons in the brain stem of the chinchilla after auditory overstimulation. Hear Res. 103:169–191. 1997. View Article : Google Scholar : PubMed/NCBI
36	Asako M, Holt AG, Griffith RD, Buras ED and Altschuler RA: Deafness-related decreases in glycine-immunoreactive labeling in the rat cochlear nucleus. J Neurosci Res. 81:102–109. 2005. View Article : Google Scholar : PubMed/NCBI
37	Spirou GA and Berrebi AS: Glycine immunoreactivity in the lateral nucleus of the trapezoid body of the cat. J Comp Neurol. 383:473–488. 1997. View Article : Google Scholar : PubMed/NCBI
38	Zhang S and Oertel D: Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. J Neurophysiol. 71:914–930. 1994.PubMed/NCBI
39	Boudreau JC and Tsuchitani C: Cat superior olive s-segment cell discharge to tonal stimulation. Contrib Sens Physiol. 4:143–213. 1970. View Article : Google Scholar : PubMed/NCBI
40	Lévi S, Vannier C and Triller A: Strychnine-sensitive stabilization of postsynaptic glycine receptor clusters. J Cell Sci. 111:335–345. 1998.PubMed/NCBI