Gap Pre-pulse Inhibition of the Cortical Auditory Evoked Potentials as a Possible Objective Pinnitus Assessment Tool
Iranian Journal of Child Neurology,
Vol. 17 No. 4 (2023),
26 October 2023
,
Page 117-136
https://doi.org/10.22037/ijcn.v17i4.42300
Abstract
Objectives
The objective assessment tests overcome the variability of subjective methods. Cortical recordings with gap pre-pulse inhibition of the acoustic startle reflex stimulus have been used as objective tinnitus assessments in humans. This study aims to investigate this possible objective tinnitus test and compare gap-induced inhibition in different stimulus parameters and brain regions.
Materials & Methods
Twenty People (18-50 years old) without hearing loss and tinnitus were included. The sound stimuli consisted of continuous background noise with a loud startle tone preceded by a silent gap (20 and 40 ms duration, 120 and 150 ms distance from the startle). The N1-P2 complex amplitude and topoplot maps were extracted in 27-channel cortical response recording after signal processing. Four brain regions of interest (ROI) of anterio-frontal, centro-frontal, right, and left temporal were investigated.
Results
The results showed that the maximum inhibition occurred in a 40 ms gap duration and 150 ms distance in all 4 ROIs. In comparing ROIs, the centro-frontal and left temporal regions revealed the most inhibition (p<0.05). The decrease in the amplitude of the N1 and P2 in that region could also be traced in the 100 and 200 ms topoplots.
Conclusion
Gap-induced inhibition was observed in all gap-embedded stimuli and all ROIs. However, the 40-150 mode and centro-frontal and left temporal regions had maximum inhibition in normal subjects. It provides a promising tool for objectively assessing tinnitus in humans with particular implications in children
- gap pre-pulse inhibition of the acoustic startle reflex, objective tinnitus assessment, cortical auditory evoked potentials
How to Cite
References
2. Lee DY, Lee JY, Kim YH. Management of tinnitus in children: Review of literature and effect of counseling. Auris Nasus Larynx. 2018;45(4):667-72.
https://doi.org/10.1016/j.anl.2017.09.002.
3. Tunkel DE, Bauer CA, Sun GH, Rosenfeld RM, Chandrasekhar SS, Cunningham ER, et al. Clinical Practice Guideline: Tinnitus. Otolaryngology–Head and Neck Surgery. 2014;151(25):S1–S40.
https://doi.org/10.1177/0194599814545325.
4. Ogawa K, Sato H, Takahashi M, Wada T, Naito Y, Kawase T, et al. Clinical practice guidelines for diagnosis and treatment of chronic tinnitus in Japan. Auris Nasus Larynx. 2020;47(1):1-6.
https://doi.org/10.1016/j.anl.2019.09.007.
5. Genitsaridi E, Hoare DJ, Kypraios T, Hall DA. A Review and a Framework of Variables for Defining and Characterizing Tinnitus Subphenotypes. brain sciences. 2020;10(12):938
https://doi.org/10.3390/brainsci10120938.
6. Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K, Hughes LF, et al. Gap Detection Deficits in Rats With Tinnitus: A Potential Novel Screening Tool. Behavioral Neuroscience. 2006;120(1):188–95.
7. Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R, et al. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hearing Research. 2007;226(1-2):244-53
DOI: 10.1016/j.heares.2006.06.013.
8. Turner JG, Parrish J. Gap Detection Methods for Assessing Salicylate-Induced Tinnitus and Hyperacusis in Rats. American Journal of Audiology. 2008;17:185-92.
9. Berger JI, Coomber B, Shackleton TM, Palmer AR, Wallace MN. A novel behavioural approach to detecting tinnitus in the guinea pig. Journal of Neuroscience Methods. 2013;213(2):188-95
https://doi.org/10.1016/j.jneumeth.2012.12.023.
10. Dehmel S, Eisinger D, Shore SE. Gap prepulse inhibition and auditory brainstem-evoked potentials as objective measures for tinnitus in guinea pigs. Frontiers in Systems Neuroscience. 2012;6.
11. Fournier P, Hébert S. Gap detection deficits in humans with tinnitus as assessed with the acoustic startle paradigm: Does tinnitus fill in the gap? Hearing Research. 2013;295:16-23.
https://doi.org/10.1016/j.heares.2012.05.011.
12. Shadwick K, Sun W. Acoustic startle reflex and pre-pulse inhibition in tinnitus patients. journal of otology. 2014;9:141-5.
https://doi.org/10.1016/j.joto.2014.12.003.
13. Campolo J, Lobarinas E, Salvi R. Does tinnitus “fill in” the silent gaps? Noise Health. 2013;15(67):https://doi.org/10.4103/1463-741.121232.
14. Wilson CA, Berger JI, Boer Jd, Sereda M, Palmer AR, Hall DA, et al. Gap-induced inhibition of the post-auricular muscle response in humans and guinea pigs. Hearing Research. 2019;374:13-23.
https://doi.org/10.1016/j.heares.2019.01.009.
15. KU Y, AHN JW, KWON C, SUH M-W, LEE JH, OH SH, et al. Gap prepulse inhibition of the auditory late response in healthy subjects. Psychophysiology. 2015;52:1511–9.
16. Burkard RF, Don M, Eggermont JJ. Auditory Evoked Potentials : Basic Principles and Clinical Application. Philadelphia, United States: Lippincott Williams and Wilkins; 2006.
17. Ku Y, Ahn Jw, Kwon C, Kim DY, Suh M-W, Park MK, et al. The gap-prepulse inhibition deficit of the cortical N1-P2 complex in patients with tinnitus: The effect of gap duration. Hearing Research. 2017:https://doi.org/10.1016/j.heares.2017.03.003.
18. Ku Y, Kim DY, Kwon C, Noh TS, Park MK, Lee JH, et al. Effect of age on the gap-prepulse inhibition of the cortical N1-P2 complex in humans as a step towards an objective measure of tinnitus. Plos One. 2020;15(11):e0241136
https://doi.org/10.1371/journal.pone.024116.
19. Fendt M, Li L, Yeomans JS. Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology. 2001;156:216–24.
20. Swerdlow NR, Geyer MA, Braff DL. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology. 2001;156:194–215.
21. Moreno-Paublete R, Canlon B, Cederroth CR. Differential Neural Responses Underlying the Inhibition of the Startle Response by Pre-Pulses or Gaps in Mice. Frontiers in Cellular Neuroscience 2017;11.
22. Ridder DD, Vanneste S, Weisz N, Londero A, Schlee W, Elgoyhen AB, et al. An integrative model of auditory phantom perception: Tinnitus as a unifiedpercept of interacting separable subnetworks. Neuroscience and Biobehavioral Reviews. 2014;44:16-32.
https://doi.org/10.1016/j.neubiorev.2013.03.021.
23. Mohsen S, Pourbakht A. An overview of the tinnitus network activity and its clinical implications. Auditory and Vestibular Research. 2018;27(4):171-8.
24. Weible AP, Moore AK, Liu C, deBlander L, Wu H, Kentros C, et al. Perceptual Gap Detection is Mediated by Gap Termination Responses in Auditory Cortex. Current Biology. 2014;24(13):1447–55.
https://doi.org/10.016/j.cub.2014.05.031.
25. Longenecker RJ, Kristaponyte I, Nelson GL, Young JW. Addressing variability in the acoustic startle reflex for accurate gap detection assessment. Hearing Research. 2018;363:119-35.
https://doi.org/10.1016/j.heares.2018.03.013.
26. Atcherson SR, Gould HJ, Mendel MI, Ethington CA. Auditory N1 Component to Gaps in Continuous Narrowband Noises. Ear & Hearing. 2009;30(6):687–95.
https://doi.org/10.1097/aud.0b013e3181b1354f.
27. Kadner A, Viirre E, C.Wester D, F.Walsh S, Hestenes J, Vankov A, et al. lateral inhibition in the auditory cortex: An EEG index of tinnitus? COGNITIVE NEUROSCIENCE ANDNEUROPSYCHOLOGY. 2002;13(4).
28. Ristovska L, Jachova Z, Stojcheska V. Psychoacoustic Characteristics of Tinnitus in Relation to Audiometric Profile. Archives of acoustics. 2019;44(3):419-28.
29. Katz J, Chasin M, English K, Hood LJ, Tillery KL. Handbook of Clinical Audiology. seventh ed. New York: Wolters Kluwer; 2015.
30. Zwicker E, Terhardt E. Analytical expressions for critical-band rate and critical bandwidthas a functionof frequency. The Journal of the Acoustical Society of America. 1980;68(5).
31. Li L, Du Y, Li N, Wu X, Wu Y. Top–down modulation of prepulse inhibition of the startle reflex in humans and rats. Neuroscience and Biobehavioral Reviews. 2009;33:1157–67.
https://doi.org/10.016/j.neubiorev.2009.02.001.
32. Hall JW. New Handbook for Auditory Evoked Responses. New York: Pearson education; 2007.
33. Morse K, Werff KRV. Comparison of Silent Gap in Noise Cortical Auditory Evoked Potentials in Matched Tinnitus and No-Tinnitus Control Subjects. American Journal of Audiology. 2019;28:260–73.
https://doi.org/10.1044/2018_AJA-18-0074.
34. Näätänen R, Picton TW. The N1 Wave of the Human Electric and Magnetic Response to Sound: A Review and an Analysis of the Component Structure. Psychophysiology. 1987;24(4):375-425.
35. Näätänen R, Teder W, Alho K, Lavikainen J. Auditory attention and selective input modulation: a topographical ERP study. Neuroreport. 1992;3(6):493-6
DOI:10.1097/00001756-199206000009.
36. Sadeghijam M, Talebian S, Mohsen S, Akbari M, Pourbakht A. Shannon entropy measures for EEG signals in tinnitus. Neuroscience Letters. 2021;762:136-53.
https://doi.org/10.1016/j.neulet.2021.136153.
37. Lowe AS, Walton JP. Alterations in Peripheral and Central Components of the Auditory Brainstem Response: A Neural Assay of Tinnitus. Plos One. 2015;10(2):doi.org/10.1371/journal.pone.0117228.
38. Fitzgibbons P. Temporal gap detectionin noiseasa function of frequency, bandwidth, and level. Acoustical Society of America. 1983;71(1).
39. Moore BCJ, Peters RW, Glasberg B. Detection of temporal gaps in sinusoids: Effects of frequency and level. Acoustical Society of America. 1993;93(3).
40. Boyen K, Başkent D, Dijk Pv. The Gap Detection Test: Can It Be Used to Diagnose Tinnitus? Ear & Hearing. 2015;36(4):138-45.
https://doi.org/10.1097/aud.0000000000000156.
41. Braff DL, Geyer MA, Swerdlow NR. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology. 2001;156:234–58.
https://doi.org/10.1007/s002130100810.
42. Geyer MA, Swerdlow NR. Measurement of Startle Response, Prepulse Inhibition, and Habituation. Current Protocols in Neuroscience. 1998.
43. E.Dawson M, Hazlett EA, Filion DL, Nuechterlein KH, Anne M. Schell. Attention and schizophrenia: Impaired modulation of the startle reflex. Journal of Abnormal Psychology. 1993;102:633-41
https://doi.org/10.1037/0021-843X.102.4.633.
44. Verkindt C, Bertrand O, Perrin F, Echallier J-F, Pernier J. Tonotopic organization of the human auditory cortex: N100 topography and multiple dipole model analysis. Electroencephalographyand clinical Neurophysiolog. 1995;96:143-56.
45. Boutros NN, Gjini K, Eickhoff SB, Urbach H, E.Pfliegerd M. Mapping repetition suppression of the P50 evoked response to the human cerebral cortex. clinical Neurophysiology. 2013;124(4):675-85.
46. Cardon E, Joossen I, Vermeersch H, Jacquemin L, Mertens G, Vanderveken OM, et al. Systematic review and meta-analysis of late auditory evoked potentials as a candidate biomarker in the assessment of tinnitus. Plos One. 2020;17:https://doi.org/10.1371/journal.pone.0243785.
1. Bhatt JM, Lin HW, Bhattacharyya N. Tinnitus Epidemiology: Prevalence, Severity, Exposures And Treatment Patterns In The United States. JAMA Otolaryngol Head Neck Surg. 2016;142(10):959–65 . https://doi.org/10.1001/jamaoto.2016.1700.
2. Lee DY, Lee JY, Kim YH. Management of tinnitus in children: Review of literature and effect of counseling. Auris Nasus Larynx. 2018;45(4):667-72.
https://doi.org/10.1016/j.anl.2017.09.002.
3. Tunkel DE, Bauer CA, Sun GH, Rosenfeld RM, Chandrasekhar SS, Cunningham ER, et al. Clinical Practice Guideline: Tinnitus. Otolaryngology–Head and Neck Surgery. 2014;151(25):S1–S40.
https://doi.org/10.1177/0194599814545325.
4. Ogawa K, Sato H, Takahashi M, Wada T, Naito Y, Kawase T, et al. Clinical practice guidelines for diagnosis and treatment of chronic tinnitus in Japan. Auris Nasus Larynx. 2020;47(1):1-6.
https://doi.org/10.1016/j.anl.2019.09.007.
5. Genitsaridi E, Hoare DJ, Kypraios T, Hall DA. A Review and a Framework of Variables for Defining and Characterizing Tinnitus Subphenotypes. brain sciences. 2020;10(12):938
https://doi.org/10.3390/brainsci10120938.
6. Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K, Hughes LF, et al. Gap Detection Deficits in Rats With Tinnitus: A Potential Novel Screening Tool. Behavioral Neuroscience. 2006;120(1):188–95.
7. Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R, et al. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hearing Research. 2007;226(1-2):244-53
DOI: 10.1016/j.heares.2006.06.013.
8. Turner JG, Parrish J. Gap Detection Methods for Assessing Salicylate-Induced Tinnitus and Hyperacusis in Rats. American Journal of Audiology. 2008;17:185-92.
9. Berger JI, Coomber B, Shackleton TM, Palmer AR, Wallace MN. A novel behavioural approach to detecting tinnitus in the guinea pig. Journal of Neuroscience Methods. 2013;213(2):188-95
https://doi.org/10.1016/j.jneumeth.2012.12.023.
10. Dehmel S, Eisinger D, Shore SE. Gap prepulse inhibition and auditory brainstem-evoked potentials as objective measures for tinnitus in guinea pigs. Frontiers in Systems Neuroscience. 2012;6.
11. Fournier P, Hébert S. Gap detection deficits in humans with tinnitus as assessed with the acoustic startle paradigm: Does tinnitus fill in the gap? Hearing Research. 2013;295:16-23.
https://doi.org/10.1016/j.heares.2012.05.011.
12. Shadwick K, Sun W. Acoustic startle reflex and pre-pulse inhibition in tinnitus patients. journal of otology. 2014;9:141-5.
https://doi.org/10.1016/j.joto.2014.12.003.
13. Campolo J, Lobarinas E, Salvi R. Does tinnitus “fill in” the silent gaps? Noise Health. 2013;15(67):https://doi.org/10.4103/1463-741.121232.
14. Wilson CA, Berger JI, Boer Jd, Sereda M, Palmer AR, Hall DA, et al. Gap-induced inhibition of the post-auricular muscle response in humans and guinea pigs. Hearing Research. 2019;374:13-23.
https://doi.org/10.1016/j.heares.2019.01.009.
15. KU Y, AHN JW, KWON C, SUH M-W, LEE JH, OH SH, et al. Gap prepulse inhibition of the auditory late response in healthy subjects. Psychophysiology. 2015;52:1511–9.
16. Burkard RF, Don M, Eggermont JJ. Auditory Evoked Potentials : Basic Principles and Clinical Application. Philadelphia, United States: Lippincott Williams and Wilkins; 2006.
17. Ku Y, Ahn Jw, Kwon C, Kim DY, Suh M-W, Park MK, et al. The gap-prepulse inhibition deficit of the cortical N1-P2 complex in patients with tinnitus: The effect of gap duration. Hearing Research. 2017:https://doi.org/10.1016/j.heares.2017.03.003.
18. Ku Y, Kim DY, Kwon C, Noh TS, Park MK, Lee JH, et al. Effect of age on the gap-prepulse inhibition of the cortical N1-P2 complex in humans as a step towards an objective measure of tinnitus. Plos One. 2020;15(11):e0241136
https://doi.org/10.1371/journal.pone.024116.
19. Fendt M, Li L, Yeomans JS. Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology. 2001;156:216–24.
20. Swerdlow NR, Geyer MA, Braff DL. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology. 2001;156:194–215.
21. Moreno-Paublete R, Canlon B, Cederroth CR. Differential Neural Responses Underlying the Inhibition of the Startle Response by Pre-Pulses or Gaps in Mice. Frontiers in Cellular Neuroscience 2017;11.
22. Ridder DD, Vanneste S, Weisz N, Londero A, Schlee W, Elgoyhen AB, et al. An integrative model of auditory phantom perception: Tinnitus as a unifiedpercept of interacting separable subnetworks. Neuroscience and Biobehavioral Reviews. 2014;44:16-32.
https://doi.org/10.1016/j.neubiorev.2013.03.021.
23. Mohsen S, Pourbakht A. An overview of the tinnitus network activity and its clinical implications. Auditory and Vestibular Research. 2018;27(4):171-8.
24. Weible AP, Moore AK, Liu C, deBlander L, Wu H, Kentros C, et al. Perceptual Gap Detection is Mediated by Gap Termination Responses in Auditory Cortex. Current Biology. 2014;24(13):1447–55.
https://doi.org/10.016/j.cub.2014.05.031.
25. Longenecker RJ, Kristaponyte I, Nelson GL, Young JW. Addressing variability in the acoustic startle reflex for accurate gap detection assessment. Hearing Research. 2018;363:119-35.
https://doi.org/10.1016/j.heares.2018.03.013.
26. Atcherson SR, Gould HJ, Mendel MI, Ethington CA. Auditory N1 Component to Gaps in Continuous Narrowband Noises. Ear & Hearing. 2009;30(6):687–95.
https://doi.org/10.1097/aud.0b013e3181b1354f.
27. Kadner A, Viirre E, C.Wester D, F.Walsh S, Hestenes J, Vankov A, et al. lateral inhibition in the auditory cortex: An EEG index of tinnitus? COGNITIVE NEUROSCIENCE ANDNEUROPSYCHOLOGY. 2002;13(4).
28. Ristovska L, Jachova Z, Stojcheska V. Psychoacoustic Characteristics of Tinnitus in Relation to Audiometric Profile. Archives of acoustics. 2019;44(3):419-28.
29. Katz J, Chasin M, English K, Hood LJ, Tillery KL. Handbook of Clinical Audiology. seventh ed. New York: Wolters Kluwer; 2015.
30. Zwicker E, Terhardt E. Analytical expressions for critical-band rate and critical bandwidthas a functionof frequency. The Journal of the Acoustical Society of America. 1980;68(5).
31. Li L, Du Y, Li N, Wu X, Wu Y. Top–down modulation of prepulse inhibition of the startle reflex in humans and rats. Neuroscience and Biobehavioral Reviews. 2009;33:1157–67.
https://doi.org/10.016/j.neubiorev.2009.02.001.
32. Hall JW. New Handbook for Auditory Evoked Responses. New York: Pearson education; 2007.
33. Morse K, Werff KRV. Comparison of Silent Gap in Noise Cortical Auditory Evoked Potentials in Matched Tinnitus and No-Tinnitus Control Subjects. American Journal of Audiology. 2019;28:260–73.
https://doi.org/10.1044/2018_AJA-18-0074.
34. Näätänen R, Picton TW. The N1 Wave of the Human Electric and Magnetic Response to Sound: A Review and an Analysis of the Component Structure. Psychophysiology. 1987;24(4):375-425.
35. Näätänen R, Teder W, Alho K, Lavikainen J. Auditory attention and selective input modulation: a topographical ERP study. Neuroreport. 1992;3(6):493-6
DOI:10.1097/00001756-199206000009.
36. Sadeghijam M, Talebian S, Mohsen S, Akbari M, Pourbakht A. Shannon entropy measures for EEG signals in tinnitus. Neuroscience Letters. 2021;762:136-53.
https://doi.org/10.1016/j.neulet.2021.136153.
37. Lowe AS, Walton JP. Alterations in Peripheral and Central Components of the Auditory Brainstem Response: A Neural Assay of Tinnitus. Plos One. 2015;10(2):doi.org/10.1371/journal.pone.0117228.
38. Fitzgibbons P. Temporal gap detectionin noiseasa function of frequency, bandwidth, and level. Acoustical Society of America. 1983;71(1).
39. Moore BCJ, Peters RW, Glasberg B. Detection of temporal gaps in sinusoids: Effects of frequency and level. Acoustical Society of America. 1993;93(3).
40. Boyen K, Başkent D, Dijk Pv. The Gap Detection Test: Can It Be Used to Diagnose Tinnitus? Ear & Hearing. 2015;36(4):138-45.
https://doi.org/10.1097/aud.0000000000000156.
41. Braff DL, Geyer MA, Swerdlow NR. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology. 2001;156:234–58.
https://doi.org/10.1007/s002130100810.
42. Geyer MA, Swerdlow NR. Measurement of Startle Response, Prepulse Inhibition, and Habituation. Current Protocols in Neuroscience. 1998.
43. E.Dawson M, Hazlett EA, Filion DL, Nuechterlein KH, Anne M. Schell. Attention and schizophrenia: Impaired modulation of the startle reflex. Journal of Abnormal Psychology. 1993;102:633-41
https://doi.org/10.1037/0021-843X.102.4.633.
44. Verkindt C, Bertrand O, Perrin F, Echallier J-F, Pernier J. Tonotopic organization of the human auditory cortex: N100 topography and multiple dipole model analysis. Electroencephalographyand clinical Neurophysiolog. 1995;96:143-56.
45. Boutros NN, Gjini K, Eickhoff SB, Urbach H, E.Pfliegerd M. Mapping repetition suppression of the P50 evoked response to the human cerebral cortex. clinical Neurophysiology. 2013;124(4):675-85.
46. Cardon E, Joossen I, Vermeersch H, Jacquemin L, Mertens G, Vanderveken OM, et al. Systematic review and meta-analysis of late auditory evoked potentials as a candidate biomarker in the assessment of tinnitus. Plos One. 2020;17:https://doi.org/10.1371/journal.pone.0243785.
1. Bhatt JM, Lin HW, Bhattacharyya N. Tinnitus Epidemiology: Prevalence, Severity, Exposures And Treatment Patterns In The United States. JAMA Otolaryngol Head Neck Surg. 2016;142(10):959–65 . https://doi.org/10.1001/jamaoto.2016.1700.
2. Lee DY, Lee JY, Kim YH. Management of tinnitus in children: Review of literature and effect of counseling. Auris Nasus Larynx. 2018;45(4):667-72.
https://doi.org/10.1016/j.anl.2017.09.002.
3. Tunkel DE, Bauer CA, Sun GH, Rosenfeld RM, Chandrasekhar SS, Cunningham ER, et al. Clinical Practice Guideline: Tinnitus. Otolaryngology–Head and Neck Surgery. 2014;151(25):S1–S40.
https://doi.org/10.1177/0194599814545325.
4. Ogawa K, Sato H, Takahashi M, Wada T, Naito Y, Kawase T, et al. Clinical practice guidelines for diagnosis and treatment of chronic tinnitus in Japan. Auris Nasus Larynx. 2020;47(1):1-6.
https://doi.org/10.1016/j.anl.2019.09.007.
5. Genitsaridi E, Hoare DJ, Kypraios T, Hall DA. A Review and a Framework of Variables for Defining and Characterizing Tinnitus Subphenotypes. brain sciences. 2020;10(12):938
https://doi.org/10.3390/brainsci10120938.
6. Turner JG, Brozoski TJ, Bauer CA, Parrish JL, Myers K, Hughes LF, et al. Gap Detection Deficits in Rats With Tinnitus: A Potential Novel Screening Tool. Behavioral Neuroscience. 2006;120(1):188–95.
7. Yang G, Lobarinas E, Zhang L, Turner J, Stolzberg D, Salvi R, et al. Salicylate induced tinnitus: behavioral measures and neural activity in auditory cortex of awake rats. Hearing Research. 2007;226(1-2):244-53
DOI: 10.1016/j.heares.2006.06.013.
8. Turner JG, Parrish J. Gap Detection Methods for Assessing Salicylate-Induced Tinnitus and Hyperacusis in Rats. American Journal of Audiology. 2008;17:185-92.
9. Berger JI, Coomber B, Shackleton TM, Palmer AR, Wallace MN. A novel behavioural approach to detecting tinnitus in the guinea pig. Journal of Neuroscience Methods. 2013;213(2):188-95
https://doi.org/10.1016/j.jneumeth.2012.12.023.
10. Dehmel S, Eisinger D, Shore SE. Gap prepulse inhibition and auditory brainstem-evoked potentials as objective measures for tinnitus in guinea pigs. Frontiers in Systems Neuroscience. 2012;6.
11. Fournier P, Hébert S. Gap detection deficits in humans with tinnitus as assessed with the acoustic startle paradigm: Does tinnitus fill in the gap? Hearing Research. 2013;295:16-23.
https://doi.org/10.1016/j.heares.2012.05.011.
12. Shadwick K, Sun W. Acoustic startle reflex and pre-pulse inhibition in tinnitus patients. journal of otology. 2014;9:141-5.
https://doi.org/10.1016/j.joto.2014.12.003.
13. Campolo J, Lobarinas E, Salvi R. Does tinnitus “fill in” the silent gaps? Noise Health. 2013;15(67):https://doi.org/10.4103/1463-741.121232.
14. Wilson CA, Berger JI, Boer Jd, Sereda M, Palmer AR, Hall DA, et al. Gap-induced inhibition of the post-auricular muscle response in humans and guinea pigs. Hearing Research. 2019;374:13-23.
https://doi.org/10.1016/j.heares.2019.01.009.
15. KU Y, AHN JW, KWON C, SUH M-W, LEE JH, OH SH, et al. Gap prepulse inhibition of the auditory late response in healthy subjects. Psychophysiology. 2015;52:1511–9.
16. Burkard RF, Don M, Eggermont JJ. Auditory Evoked Potentials : Basic Principles and Clinical Application. Philadelphia, United States: Lippincott Williams and Wilkins; 2006.
17. Ku Y, Ahn Jw, Kwon C, Kim DY, Suh M-W, Park MK, et al. The gap-prepulse inhibition deficit of the cortical N1-P2 complex in patients with tinnitus: The effect of gap duration. Hearing Research. 2017:https://doi.org/10.1016/j.heares.2017.03.003.
18. Ku Y, Kim DY, Kwon C, Noh TS, Park MK, Lee JH, et al. Effect of age on the gap-prepulse inhibition of the cortical N1-P2 complex in humans as a step towards an objective measure of tinnitus. Plos One. 2020;15(11):e0241136
https://doi.org/10.1371/journal.pone.024116.
19. Fendt M, Li L, Yeomans JS. Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology. 2001;156:216–24.
20. Swerdlow NR, Geyer MA, Braff DL. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology. 2001;156:194–215.
21. Moreno-Paublete R, Canlon B, Cederroth CR. Differential Neural Responses Underlying the Inhibition of the Startle Response by Pre-Pulses or Gaps in Mice. Frontiers in Cellular Neuroscience 2017;11.
22. Ridder DD, Vanneste S, Weisz N, Londero A, Schlee W, Elgoyhen AB, et al. An integrative model of auditory phantom perception: Tinnitus as a unifiedpercept of interacting separable subnetworks. Neuroscience and Biobehavioral Reviews. 2014;44:16-32.
https://doi.org/10.1016/j.neubiorev.2013.03.021.
23. Mohsen S, Pourbakht A. An overview of the tinnitus network activity and its clinical implications. Auditory and Vestibular Research. 2018;27(4):171-8.
24. Weible AP, Moore AK, Liu C, deBlander L, Wu H, Kentros C, et al. Perceptual Gap Detection is Mediated by Gap Termination Responses in Auditory Cortex. Current Biology. 2014;24(13):1447–55.
https://doi.org/10.016/j.cub.2014.05.031.
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