Intracranial Mapping of a Cortical Tinnitus System using Residual Inhibition

William Sedley; Phillip E Gander; Sukhbinder Kumar; Hiroyuki Oya; Christopher K Kovach; Kirill V Nourski; Hiroto Kawasaki; Matthew A Howard; Timothy D Griffiths

doi:10.1016/j.cub.2015.02.075

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Intracranial Mapping of a Cortical Tinnitus System using Residual Inhibition

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Intracranial Mapping of a Cortical Tinnitus System using Residual Inhibition

William Sedley, Phillip E Gander, Sukhbinder Kumar, Hiroyuki Oya, Christopher K Kovach, Kirill V Nourski, Hiroto Kawasaki, Matthew A Howard and Timothy D Griffiths

Current biology, Vol.25(9), pp.1208-1214

05/04/2015

DOI: 10.1016/j.cub.2015.02.075

PMCID: PMC4425458

PMID: 25913402

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Abstract

Tinnitus can occur when damage to the peripheral auditory system leads to spontaneous brain activity that is interpreted as sound [ 1, 2 ]. Many abnormalities of brain activity are associated with tinnitus, but it is unclear how these relate to the phantom sound itself, as opposed to predisposing factors or secondary consequences [ 3 ]. Demonstrating “core” tinnitus correlates (processes that are both necessary and sufficient for tinnitus perception) requires high-precision recordings of neural activity combined with a behavioral paradigm in which the perception of tinnitus is manipulated and accurately reported by the subject. This has been previously impossible in animal and human research. Here we present extensive intracranial recordings from an awake, behaving tinnitus patient during short-term modifications in perceived tinnitus loudness after acoustic stimulation (residual inhibition) [ 4 ], permitting robust characterization of core tinnitus processes. As anticipated, we observed tinnitus-linked low-frequency (delta) oscillations [ 5–9 ], thought to be triggered by low-frequency bursting in the thalamus [ 10, 11 ]. Contrary to expectation, these delta changes extended far beyond circumscribed auditory cortical regions to encompass almost all of auditory cortex, plus large parts of temporal, parietal, sensorimotor, and limbic cortex. In discrete auditory, parahippocampal, and inferior parietal “hub” regions [ 12 ], these delta oscillations interacted with middle-frequency (alpha) and high-frequency (beta and gamma) activity, resulting in a coherent system of tightly coupled oscillations associated with high-level functions including memory and perception. • Extensive intracranial recordings were made from an awake, behaving tinnitus patient • Tinnitus intensity was modulated with tight control over other factors • Tinnitus is linked to widespread coherent delta-band cortical oscillations • Rich local cross-frequency interactions link delta to all other frequency bands Recording from an extensive array of intracranial electrodes in an awake, behaving human patient, Sedley, Gander et al. expose the detailed workings of a brain system responsible for generating tinnitus.

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Title: Subtitle: Intracranial Mapping of a Cortical Tinnitus System using Residual Inhibition
Creators: William Sedley - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Phillip E Gander - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Sukhbinder Kumar - Auditory Group, Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, Tyne and Wear NE2 4HH, UK
Hiroyuki Oya - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Christopher K Kovach - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Kirill V Nourski - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Hiroto Kawasaki - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Matthew A Howard - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Timothy D Griffiths - Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA
Resource Type: Journal article
Publication Details: Current biology, Vol.25(9), pp.1208-1214
DOI: 10.1016/j.cub.2015.02.075
PMID: 25913402
PMCID: PMC4425458
NLM abbreviation: Curr Biol
ISSN: 0960-9822
eISSN: 1879-0445
Publisher: Cell Press
Language: English
Date published: 05/04/2015
Academic Unit: Neurology; Psychological and Brain Sciences; Iowa Neuroscience Institute; Neurosurgery; Otolaryngology
Record Identifier: 9984020615102771

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