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Long-Lasting forward Suppression of Spontaneous Firing in Auditory Neurons: Implication to the Residual Inhibition of Tinnitus

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Abstract

Tinnitus is the perception of a sound that has no external source. Sound stimuli can suppress spontaneous firing in auditory neurons long after stimulus offset. It is unknown how changes in sound stimulus parameters affect this forward suppression. Using in vivo extracellular recording in awake mice, we found that about 40 % of spontaneously active inferior colliculus (IC) neurons exhibited forward suppression of spontaneous activity after sound offset. The duration of this suppression increased with sound duration and lasted about 40 s following a 30-s stimulus offset. Pure tones presented at the neuron’s characteristic frequency (CF) were more effective in triggering suppression compared to non-CF or wideband noise stimuli. In contrast, non-CF stimuli often induced forward facilitation. About one third of IC neurons exhibited shorter suppression durations with each subsequent sound presentation. These characteristics of forward suppression are similar to the psychoacoustic properties of residual inhibition of tinnitus: a phenomenon of brief (about 30 s) suppression of tinnitus observed in tinnitus patients after sound presentations. Because elevated spontaneous firing in central auditory neurons has been linked to tinnitus, forward suppression of this firing with sound might be an underlying mechanism of residual inhibition.

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Abbreviations

RI:

Residual inhibition

IC:

Inferior colliculus

AC:

Auditory cortex

CF:

Characteristic frequency

PSTH:

Peristimulus time histogram

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Acknowledgments

We would like to acknowledge Dr. Larry Roberts, Dr. Arnaud Noreña, Dr. Merri Rosen, Inga Kristaponyte, and Greg Nelson for their comments on earlier versions of this manuscript. This research was supported by grant R01 DC011330 to A.V. Galazyuk and F31 DC013498-01A1 to R. J. Longenecker from the National Institute on Deafness and Other Communication Disorders of the US Public Health Service.

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Authors and Affiliations

  1. Department of Anatomy and Neurobiology, Northeast Ohio Medical University, 4209 State Route 44, Rootstown, OH, 44272, USA

    A. V. Galazyuk & R. J. Longenecker

  2. Department of Neuronal Networks Physiology, Bogomoletz Institute of Physiology, National Academy of Sciences of Ukraine, Kiev, Ukraine

    S. V. Voytenko

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  1. A. V. Galazyuk
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  2. S. V. Voytenko
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Correspondence to A. V. Galazyuk.

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All procedures used in this study were approved by the Institutional Animal Care and Use Committee at Northeast Ohio Medical University.

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The authors declare that they have no conflict of interest.

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Galazyuk, A.V., Voytenko, S.V. & Longenecker, R.J. Long-Lasting forward Suppression of Spontaneous Firing in Auditory Neurons: Implication to the Residual Inhibition of Tinnitus. JARO 18, 343–353 (2017). https://doi.org/10.1007/s10162-016-0601-9

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  • DOI: https://doi.org/10.1007/s10162-016-0601-9

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