Tinnitus and temporary hearing loss result in differential noise-induced spatial reorganization of brain activity

Abstract

Loud noise frequently results in hyperacusis or hearing loss (i.e., increased or decreased sensitivity to sound). These conditions are often accompanied by tinnitus (ringing in the ears) and changes in spontaneous neuronal activity (SNA). The ability to differentiate the contributions of hyperacusis and hearing loss to neural correlates of tinnitus has yet to be achieved. Towards this purpose, we used a combination of behavior, electrophysiology, and imaging tools to investigate two models of noise-induced tinnitus (either with temporary hearing loss or with permanent hearing loss). Manganese (Mn2+) uptake was used as a measure of calcium channel function and as an index of SNA. Manganese uptake was examined in vivo with manganese-enhanced magnetic resonance imaging (MEMRI) in key auditory brain regions implicated in tinnitus. Following acoustic trauma, MEMRI, the SNA index, showed evidence of spatially dependent rearrangement of Mn2+ uptake within specific brain nuclei (i.e., reorganization). Reorganization of Mn2+ uptake in the superior olivary complex and cochlear nucleus was dependent upon tinnitus status. However, reorganization of Mn2+ uptake in the inferior colliculus was dependent upon hearing sensitivity. Furthermore, following permanent hearing loss, reduced Mn2+ uptake was observed. Overall, by combining testing for hearing sensitivity, tinnitus, and SNA, our data move forward the possibility of discriminating the contributions of hyperacusis and hearing loss to tinnitus.

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Acknowledgements

We thank Mohanned Ahmed, Ahmad Ali Nassar, Sharowyn Wilson, and Nour Arafat for their help with experiments, analysis and creating macros for data analysis. A special thank you to Drs. P. D. Walker and R. Braun for providing feedback on the article prior to submission.

Funding

This work was supported by the Department of Veterans Affairs (Grant 1I01RX001095-01U.S to A.G.H); the National Institute for Occupational Safety and Health, Centers for Disease Control and Prevention (training Grant T42 OH008455 to AGH and AKA); the National Institutes of Health (Grant EY021619 to BAB); and Research to Prevent Blindness (unrestricted Grant to BAB). The views expressed do not necessarily reflect the official policies of the Department of Health and Human Services, nor does mention of trade names, commercial practices, or organizations imply endorsement by the US Government.

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Correspondence to Avril Genene Holt.

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Muca, A., Standafer, E., Apawu, A.K. et al. Tinnitus and temporary hearing loss result in differential noise-induced spatial reorganization of brain activity. Brain Struct Funct 223, 2343–2360 (2018). https://doi.org/10.1007/s00429-018-1635-z

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Keywords

  • Tinnitus
  • Hyperacusis
  • Neuronal activity
  • Hyperactivity
  • Neuroplasticity
  • Hearing loss
  • Permanent threshold shift
  • Temporary threshold shift
  • Manganese enhanced MRI
  • Gap detection
  • MEMRI
  • Acoustic startle reflex