Abstract
Tinnitus is a symptom of various disorders that affects the quality of life of millions people. Given the significance of the access to an objective and non-invasive method for tinnitus detection, in this study the auditory brainstem response (ABR) electrophysiological test was used to diagnose salicylate-induced tinnitus, in parallel with common behavioral tests. Wistar rats were divided into saline (n = 7), and salicylate (n = 7) groups for behavioral tests, and salicylate group (n = 5) for the ABR test. The rats were evaluated by pre-pulse inhibition (PPI), gap pre-pulse inhibition of the acoustic startle (GPIAS), and ABR tests, at baseline, 14 and 62 h after salicylate (350 mg/kg) or vehicle injection. The mean percentage of GPIAS test was significantly reduced following salicylate administration, which confirms the induction of tinnitus. The ABR test results showed an increase in the hearing threshold at click and 8, 12, and 16 kHz tones. Moreover, a decline was observed in the latency ratio of II-I waves in all tone burst frequencies with the highest variation in 12 and 16 kHz as well as a decrement in the latency ratio of III-I and IV-I only in 12 and 16 kHz. ABR test is able to evaluate the salicylate induced tinnitus pitch and confirm the results of behavioral tinnitus tests. GPIAS reflexive response is dependent on brainstem circuits and the auditory cortex while, ABR test can demonstrate the function of the auditory brainstem in more details, and therefore, a combination of these two tests can offer a more accurate tinnitus evaluation.
Graphical Abstract
Similar content being viewed by others
References
Domarecka E, Olze H, Szczepek AJ (2020) Auditory Brainstem Responses (ABR) of rats during experimentally induced tinnitus: literature review. Brain Sci 10(12):901. https://doi.org/10.3390/brainsci10120901
Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R et al (2007) Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hear Res 226(1–2):244–253. https://doi.org/10.1016/j.heares.2006.06.013
Fang L, Fu Y, Zhang T-y (2016) Salicylate-Induced hearing loss trigger structural synaptic modifications in the ventral cochlear nucleus of rats via medial olivocochlear (MOC) feedback circuit. Neurochem Res 41(6):1343–1353. https://doi.org/10.1007/s11064-016-1836-x
Yi B, Hu S, Zuo C, Jiao F, Lv J, Chen D et al (2016) Effects of long-term salicylate administration on synaptic ultrastructure and metabolic activity in the rat CNS. Sci Rep 6(1):1–11. https://doi.org/10.1038/srep24428
Ralli M, Troiani D, Podda MV, Paciello F, Eramo S, De Corso E et al (2014) The effect of the NMDA channel blocker memantine on salicylate-induced tinnitus in rats. Acta Otorhinolaryngol Ital 34(3):198 (PMID: 24882929)
Berger JI, Coomber B, Shackleton TM, Palmer AR, Wallace MN (2013) A novel behavioural approach to detecting tinnitus in the guinea pig. J Neurosci Methods 213(2):188–195. https://doi.org/10.1016/j.jneumeth.2012.12.023
Stolzberg D, Salvi RJ, Allman BL (2012) Salicylate toxicity model of tinnitus. Front Syst Neurosci 6:28. https://doi.org/10.3389/fnsys.2012.00028
Sawka B, Wei S (2014) The effects of salicylate on auditory evoked potential amplitwde from the auditory cortex and auditory brainstem. J Otol 9(1):30–35. https://doi.org/10.1016/S1672-2930(14)50006-2
Rezapour M, Moossavi A (2019) Tinnitus induction in animals and its impact on auditory system structure. Auditory Vestibular Res; 28(4):204–16. https://doi.org/10.18502/avr.v28i4.1455
Galazyuk A, Hébert S (2015) Gap-prepulse inhibition of the acoustic startle reflex (GPIAS) for tinnitus assessment: current status and future directions. Front Neurol 6:88. https://doi.org/10.3389/fneur.2015.00088
Lowe AS, Walton JP (2015) Alterations in peripheral and central components of the auditory brainstem response: a neural assay of tinnitus. PLoS ONE 10(2):e0117228. https://doi.org/10.1371/journal.pone.0117228
Turner JG, Parrish J (2008) Gap Detection Methods for Assessing Salicylate-Induced Tinnitus and Hyperacusis in Rats. Am J Audiol 17(2):S185–S192. https://doi.org/10.1044/1059-0889(2008/08-0006)
Martel DT, Pardo-Garcia TR, Shore SE (2019) Dorsal cochlear nucleus fusiform-cell plasticity is altered in salicylate-induced tinnitus. Neuroscience 407:170–181. https://doi.org/10.1016/j.neuroscience.2018.08.035
Berger JI, Owen W, Wilson CA, Hockley A, Coomber B, Palmer AR et al (2018) Gap-induced reductions of evoked potentials in the auditory cortex: a possible objective marker for the presence of tinnitus in animals. Brain Res 1679:101–108. https://doi.org/10.1016/j.brainres.2017.11.026
Longenecker R, Galazyuk A (2012) Methodological optimization of tinnitus assessment using prepulse inhibition of the acoustic startle reflex. Brain Res 1485:54–62. https://doi.org/10.1016/j.brainres.2012.02.067
Moreno-Paublete R, Canlon B, Cederroth CR (2017) Differential neural responses underlying the inhibition of the startle response by pre-pulses or gaps in mice. Front Cell Neurosci 11:19. https://doi.org/10.3389/fncel.2017.00019
Lauer AM, Larkin G, Jones A, May BJ (2018) Behavioral animal model of the emotional response to tinnitus and hearing loss. J Assoc Res Otolaryngol 19(1):67–81. https://doi.org/10.1007/s10162-017-0642-8
Turner J, Larsen D, Hughes L, Moechars D, Shore S (2012) Time course of tinnitus development following noise exposure in mice. J Neurosci Res 90(7):1480–1488. https://doi.org/10.1002/jnr.22827
Alvarado JC, Fuentes-Santamaría V, Jareño-Flores T, Blanco JL, Juiz JM (2012) Normal variations in the morphology of auditory brainstem response (ABR) waveforms: a study in Wistar rats. Neurosci Res 73(4):302–311. https://doi.org/10.1016/j.neures.2012.05.001
Sun W, Doolittle L, Flowers E, Zhang C, Wang Q (2014) High doses of salicylate causes prepulse facilitation of onset-gap induced acoustic startle response. Behav Brain Res 258:187–192. https://doi.org/10.1016/j.bbr.2013.10.024
Rüttiger L, Ciuffani J, Zenner H-P, Knipper M (2003) A behavioral paradigm to judge acute sodium salicylate-induced sound experience in rats: a new approach for an animal model on tinnitus. Hear Res 180(1–2):39–50. https://doi.org/10.1016/S0378-5955(03)00075-3
Liu X-P, Chen L (2015) Forward acoustic masking enhances the auditory brainstem response in a diotic, but not dichotic, paradigm in salicylate-induced tinnitus. Hear Res 323:51–60. https://doi.org/10.1016/j.heares.2015.01.013
Su Y-Y, Luo B, Jin Y, Wu S-H, Lobarinas E, Salvi RJ et al (2012) Altered neuronal intrinsic properties and reduced synaptic transmission of the rat’s medial geniculate body in salicylate-induced tinnitus. PLoS ONE. https://doi.org/10.1371/journal.pone.0046969
Leggett K, Mendis V, Mulders W (2018) Divergent responses in the gap prepulse inhibition of the acoustic startle reflex in two different guinea pig colonies. Int Tinnitus J 22(1):1–9. https://doi.org/10.5935/0946-5448.20180001
Radziwon KE, Stolzberg DJ, Urban ME, Bowler RA, Salvi RJ (2015) Salicylate-induced hearing loss and gap detection deficits in rats. Front Neurol 6:31. https://doi.org/10.3389/fneur.2015.00031
Duron J, Monconduit L, Avan P (2020) Auditory brainstem changes in timing may underlie hyperacusis in a salicylate-induced acute rat model. Neuroscience 426:129–140. https://doi.org/10.1016/j.neuroscience.2019.11.038
Castañeda R, Natarajan S, Jeong SY, Hong BN, Kang TH (2019) Electrophysiological changes in auditory evoked potentials in rats with salicylate-induced tinnitus. Brain Res 1715:235–244. https://doi.org/10.1016/j.brainres.2019.04.004
Liu X-P, Chen L (2012) Auditory brainstem response as a possible objective indicator for salicylate-induced tinnitus in rats. Brain Res 1485:88–94. https://doi.org/10.1016/j.brainres.2012.04.048
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. All the authors have read the manuscript and have approved this submission. We further confirm that any aspect of the work covered in this manuscript that has involved experimental animals has been conducted with the ethical approval of all relevant bodies and that such approvals are acknowledged within the manuscript.
Corresponding author
Ethics declarations
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Conflicts of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Ethics Approval
This study is part of Mitra Rezapour's Ph.D dissertation in the field of audiology at Iran University of Medical Sciences. All experiments were carried out based on the guide for the care and use of laboratory animals (National Institutes of Health Publication No. 80–23, revised 1978) and confirmed by the Ethics Committee of Iran University of Medical Sciences (IR.IUMS.REC.1399.402).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rezapour, M., Akbari, M., Dargahi, L. et al. The Auditory Brainstem Response (ABR) Test, Supplementary to Behavioral Tests for Evaluation of the Salicylate-Induced Tinnitus. Indian J Otolaryngol Head Neck Surg 75 (Suppl 1), 6–15 (2023). https://doi.org/10.1007/s12070-022-03117-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12070-022-03117-x