Intracranial Mapping of a Cortical Tinnitus System using Residual Inhibition.
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.
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA; Auditory Group, Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, Tyne and Wear NE2 4HH, UK. Electronic address: willsedley@gmail.com.
William
W
Sedley
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA. Electronic address: phillip-gander@uiowa.edu.
Phillip E
PE
Gander
Auditory Group, Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, Tyne and Wear NE2 4HH, UK; Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, UK.
Sukhbinder
S
Kumar
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA.
Hiroyuki
H
Oya
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA.
Christopher K
CK
Kovach
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA.
Kirill V
KV
Nourski
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA.
Hiroto
H
Kawasaki
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA.
Matthew A
MA
Howard
Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, IA 52242, USA; Auditory Group, Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, Tyne and Wear NE2 4HH, UK; Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, UK.
Timothy D
TD
Griffiths
D001303:Auditory Cortex / Q000503:physiopathology*; D001931:Brain Mapping; D006801:Humans; D008297:Male; D008875:Middle Aged; D014012:Tinnitus / Q000503:physiopathology*