Relationship Between Caudal and Rostral Auditory Efferent Pathways: A Preliminary Investigation

Authors

  • Shezeen Abdul Gafoor Junior Research Fellow
  • Ajith Kumar Professor

DOI:

https://doi.org/10.15540/nr.9.1.39

Keywords:

auditory efferent system, auditory sensory gating, ; contralateral inhibition of otoacoustic emissions, inhibition

Abstract

Perception of sounds involves excitatory as well as inhibitory activities. Inhibition occurs throughout the auditory system, from the auditory cortex to the cochlea, and is predominantly mediated by the auditory efferent system. In the present study, we assessed the interactions between two measures of inhibition in neurotypical adults—contralateral inhibition of otoacoustic emissions, which is a subcortical measure, and sensory gating, a cortical measure. We found an inverse relationship between these two functions. The possible reasons for this are discussed with an implication to the auditory efferent system.

References

Abdala, C., Dhar, S., Ahmadi, M., & Luo, P. (2014). Aging of the medial olivocochlear reflex and associations with speech perception. The Journal of the Acoustical Society of America, 135(2), 754–765. https://doi.org/10.1121/1.4861841

Adler, L. E., Pachtman, E., Franks. D., Pecevich, M., Waldo, M. C., & Freedman, R. (1982). Neurophysiologic evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biological Psychiatry, 17(6), 639–654.

Adler, L. E., Waldo, M. C., & Freedman, R. (1985). Neurophysiologic studies of sensory gating in schizophrenia: Comparison of auditory and visual responses. Biological Psychiatry, 20(12), 1284–1296. https://doi.org/10.1016/0006-3223(85)90113-1

Anderson, L. A., Christianson, G. B., & Linden, J. F. (2009). Stimulus-specific adaptation occurs in the auditory thalamus. Journal of Neuroscience, 29(22), 7359–7363. https://doi.org/10.1523/JNEUROSCI.0793-09.2009

Antunes, F. M., & Malmierca, M. S. (2021). Corticothalamic pathways in auditory processing: Recent advances and insights from other sensory systems. Frontiers in Neural Circuits, 15, 721186. https://doi.org/10.3389/fncir.2021.721186

Arciniegas, D., Olincy, A., Topkoff, J., McRae, K., Cawthra, E., Filley, C. M., Reite, M., & Adler, L. E. (2000). Impaired auditory gating and P50 nonsuppression following traumatic brain injury. The Journal of Neuropsychiatry and Clinical Neurosciences, 12(1), 77–85. https://doi.org/10.1176/jnp.12.1.77

Boutros, N. N., & Belger, A. (1999). Midlatency evoked potentials attenuation and augmentation reflect different aspects of sensory gating. Biological Psychiatry, 45(7), 917–922. https://doi.org/10.1016/S0006-3223(98)00253-4

Briggs, F., & Usrey, W. M. (2008). Emerging views of corticothalamic function. Current Opinion in Neurobiology, 18(4), 403–407. https://doi.org/10.1016/j.conb.2008.09.002

Campbell, J., Bean, C., & LaBrec, A. (2018). Normal hearing young adults with mild tinnitus: Reduced inhibition as measured through sensory gating. Audiology Research, 8(2), 27–33. https://doi.org/10.4081/audiores.2018.214

Campbell, J., Nielsen, M., Bean, C., & LaBrec, A. (2020). Auditory gating in hearing loss. Journal of the American Academy of Audiology, 31(08), 559–565. https://doi.org/10.1055/s-0040-1709517

Campbell, J., Nielsen, M., LaBrec, A., & Bean, C. (2020). Sensory inhibition is related to variable speech perception in noise in adults with normal hearing. Journal of Speech, Language, and Hearing Research, 63(5), 1595–1607. https://doi.org/10.1044/2020_JSLHR-19-00261

Collet, L., Kemp, D. T., Veuillet, E., Duclaux, R., Moulin, A., & Morgon, A. (1990). Effect of contralateral auditory stimuli on active cochlear micro-mechanical properties in human subjects. Hearing Research, 43(2–3), 251–261. https://doi.org/10.1016/0378-5955(90)90232-e

de Boer, J., & Thornton, A. R. D. (2007). Effect of subject task on contralateral suppression of click evoked otoacoustic emissions. Hearing Research, 233(1–2), 117–123. https://doi.org/10.1016/j.heares.2007.08.002

Delano, P. H., & Elgoyhen, A. B. (2016). Editorial: Auditory efferent system: New insights from cortex to cochlea. Frontiers in Systems Neuroscience, 10, 50. https://doi.org/10.3389/fnsys.2016.00050

Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009

Freedman, R., Adler, L. E., & Waldo, M. (1987). Gating of the auditory evoked potential in children and adults. Psychophysiology, 24(2), 223–227. https://doi.org/10.1111/j.1469-8986.1987.tb00282.x

Friston, K. (2005). A theory of cortical responses. Philosophical Transactions of the Royal Society B: Biological Sciences, 360(1456), 815–836. https://doi.org/10.1098/rstb.2005.1622

Fuerst, D. R., Gallinat, J., & Boutros, N. N. (2007). Range of sensory gating values and test–retest reliability in normal subjects. Psychophysiology, 44(4), 620–626. https://doi.org/10.1111/j.1469-8986.2007.00524.x

Garrido, M. I., Kilner, J. M., Kiebel, S. J., Stephan, K. E., Baldeweg, T., & Friston, K. J. (2009). Repetition suppression and plasticity in the human brain. NeuroImage, 48(1), 269–279. https://doi.org/10.1016/j.neuroimage.2009.06.034

Giraud, A. L., Garnier, S., Micheyl, C., Lina, G., Chays, A., & Chéry-Croze, S. (1997). Auditory efferents involved in speech-in-noise intelligibility. NeuroReport, 8(7), 1779–1783. https://doi.org/10.1097/00001756-199705060-00042

Guinan, J. J. (2006). Olivocochlear efferents : Anatomy, physiology, function, and the measurement of efferent effects in humans. Ear and Hearing, 27(6), 589–607. https://doi.org/10.1097/01.aud.0000240507.83072.e7

Hackney, C. M. (1987). Anatomical features of the auditory pathway from cochlea to cortex. British Medical Bulletin, 43(4), 780–801. https://doi.org/10.1093/oxfordjournals.bmb.a072218

Harkrider, A. W., & Hedrick, M. S. (2005). Acute effect of nicotine on auditory gating in smokers and non-smokers. Hearing Research, 202(1–2), 114–128. https://doi.org/10.1016/j.heares.2004.11.009

Hirano, Y., Hirano, S., Maekawa, T., Obayashi, C., Oribe, N., Monji, A., Kasai, K., Kanba, S., & Onitsuka, T. (2010). Auditory gating deficit to human voices in schizophrenia: A MEG study. Schizophrenia Research, 117(1), 61–67. https://doi.org/10.1016/j.schres.2009.09.003

Kerby, D. S. (2014). The simple difference formula: An approach to teaching nonparametric correlation. Comprehensive Psychology, 3, 11.IT. https://doi.org/10.2466/11.IT.3.1

Kumar, U. A., Hegde, M., & Mayaleela. (2010). Perceptual learning of non-native speech contrast and functioning of the olivocochlear bundle. International Journal of Audiology, 49(7), 488–496. https://doi.org/10.3109/14992021003645894

Kumar, U. A., & Vanaja, C. S. (2004). Functioning of olivocochlear bundle and speech perception in noise. Ear and Hearing, 25(2), 142–146. https://doi.org/10.1097/01.AUD.0000120363.56591.E6

Lijffijt, M., Moeller, F. G., Boutros, N. N., Steinberg, J. L., Meier, S. L., Lane, S. D., & Swann, A. C. (2009). Diminished P50, N100 and P200 auditory sensory gating in bipolar I disorder. Psychiatry Research, 167(3), 191–201. https://doi.org/10.1016/j.psychres.2008.04.001

Ma, X., & Suga, N. (2001). Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proceedings of the National Academy of Sciences of the United States of America, 98(24), 14060–14065. https://doi.org/10.1073/pnas.241517098

Malmierca, M. S., Anderson, L. A., & Antunes, F. M. (2015). The cortical modulation of stimulus-specific adaptation in the auditory midbrain and thalamus: A potential neuronal correlate for predictive coding. Frontiers in Systems Neuroscience, 9, 19. https://doi.org/10.3389/fnsys.2015.00019

Maruthy, S., Kumar, U. A., & Gnanateja, G. N. (2017). Functional interplay between the putative measures of rostral and caudal efferent regulation of speech perception in noise. Journal of the Association for Research in Otolaryngology, 18(4), 635–648. https://doi.org/10.1007/s10162-017-0623-y

Maruthy, S., Kumar, U. A., & Gnanateja, N. (2012). Neuro-physiological mechanisms of speech perception in noise [Unpublished Departmental Project]. All India Institute of Speech and Hearing, University of Mysore. http://aiish.ac.in/digital-library.html

Mayer, A. R., Hanlon, F. M., Franco, A. R., Teshiba, T. M., Thoma, R. J., Clark, V. P., & Canive, J. M. (2009). The neural networks underlying auditory sensory gating. NeuroImage, 44(1), 182–189. https://doi.org/10.1016/j.neuroimage.2008.08.025

Mertes, I. B., Johnson, K. M., & Dinger, Z. A. (2019). Olivocochlear efferent contributions to speech-in-noise recognition across signal-to-noise ratios. The Journal of the Acoustical Society of America, 145(3), 1529–1540. https://doi.org/10.1121/1.5094766

O’Reilly, J. A. (2021). Roving oddball paradigm elicits sensory gating, frequency sensitivity, and long-latency response in common marmosets. IBRO Neuroscience Reports, 11, 128–136. https://doi.org/10.1016/j.ibneur.2021.09.003

Patterson, J. V., Hetrick, W. P., Boutros, N. N., Jin, Y., Sandman, C., Stern, H., Potkin, S., & Bunney, W. E. (2008). P50 sensory gating ratios in schizophrenics and controls: A review and data analysis. Psychiatry Research, 158(2), 226–247. https://doi.org/10.1016/j.psychres.2007.02.009

Rentzsch, J., Gomez-Carrillo de Castro, A., Neuhaus, A., Jockers-Scherübl, M. C., & Gallinat, J. (2008). Comparison of midlatency auditory sensory gating at short and long interstimulus intervals. Neuropsychobiology, 58(1), 11–18. https://doi.org/10.1159/000154475

Rentzsch, J., Jockers-Scherübl, M. C., Boutros, N. N., & Gallinat, J. (2008). Test–retest reliability of P50, N100 and P200 auditory sensory gating in healthy subjects. International Journal of Psychophysiology, 67(2), 81–90. https://doi.org/10.1016/j.ijpsycho.2007.10.006

Riga, M., Papadas, T., Werner, J. A., & Dalchow, C. V. (2007). A clinical study of the efferent auditory system in patients with normal hearing who have acute tinnitus. Otology & Neurotology, 28(2), 185–190. https://doi.org/10.1097/MAO.0b013e31802e2a14

Smith, D. M., Grant, B., Fisher, D. J., Borracci, G., Labelle, A., & Knott, V. J. (2013). Auditory verbal hallucinations in schizophrenia correlate with P50 gating. Clinical Neurophysiology, 124(7), 1329–1335. https://doi.org/10.1016/j.clinph.2013.02.004

Stuart, A., & Kerls, A. N. (2018). Does contralateral inhibition of transient evoked otoacoustic emissions suggest sex or ear laterality effects? American Journal of Audiology, 27(3), 272–282. https://doi.org/10.1044/2018_AJA-17-0106

Suga, N. (2020). Plasticity of the adult auditory system based on corticocortical and corticofugal modulations. Neuroscience & Biobehavioral Reviews, 113, 461–478. https://doi.org/10.1016/j.neubiorev.2020.03.021

Suga, N., Gao, E., Zhang, Y., Ma, X., & Olsen, J. F. (2000). The corticofugal system for hearing: Recent progress. Proceedings of the National Academy of Sciences of the United States of America, 97(22), 11807–11814. https://doi.org/10.1073/pnas.97.22.11807

Takaura, K., & Fujii, N. (2016). Facilitative effect of repetitive presentation of one stimulus on cortical responses to other stimuli in macaque monkeys—a possible neural mechanism for mismatch negativity. European Journal of Neuroscience, 43(4), 516–528. https://doi.org/10.1111/ejn.13136

Tang, J., Yang, W., & Suga, N. (2012). Modulation of thalamic auditory neurons by the primary auditory cortex. Journal of Neurophysiology, 108(3), 935–942. https://doi.org/10.1152/jn.00251.2012

Terreros, G., & Delano, P. H. (2015). Corticofugal modulation of peripheral auditory responses. Frontiers in Systems Neuroscience, 9, 134. https://doi.org/10.3389/fnsys.2015.00134

Todorovic, A., & de Lange, F. P. (2012). Repetition suppression and expectation suppression are dissociable in time in early auditory evoked fields. The Journal of Neuroscience, 32(39), 13389–13395. https://doi.org/10.1523/JNEUROSCI.2227-12.2012

Venkatesan, S., & Basavaraj, V. (2009). Ethical Guidelines for Bio-Behavioral Research Involving Human Subjects, 1–23. Mysore, India: All India Institute of Speech & Hearing. http://www.aiishmysore.in/en/pdf/ethical_guidelines.pdf

Wahab, N. A. A., Wahab, S., Rahman, A. H. A., Sidek, D., & Zakaria, M. N. (2016). The hyperactivity of efferent auditory system in patients with schizophrenia: A transient evoked otoacoustic emissions study. Psychiatry Investigation, 13(1), 82–88. https://doi.org/10.4306/pi.2016.13.1.82

Yan, J., & Ehret, G. (2002). Corticofugal modulation of midbrain sound processing in the house mouse. European Journal of Neurosciences, 16(1), 119–128. https://doi.org/10.1046/j.1460-9568.2002.02046.x

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Published

2022-03-27

Issue

Vol. 9 No. 1 (2022)

Section

Research Papers

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