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A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex

The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschl's gyrus (HG) with pronounced induced h...

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Autores principales: Billig, Alexander J., Herrmann, Björn, Rhone, Ariane E., Gander, Phillip E., Nourski, Kirill V., Snoad, Beau F., Kovach, Christopher K., Kawasaki, Hiroto, Howard, Matthew A., Johnsrude, Ingrid S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6820204/
https://www.ncbi.nlm.nih.gov/pubmed/31533976
http://dx.doi.org/10.1523/JNEUROSCI.0696-19.2019
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author Billig, Alexander J.
Herrmann, Björn
Rhone, Ariane E.
Gander, Phillip E.
Nourski, Kirill V.
Snoad, Beau F.
Kovach, Christopher K.
Kawasaki, Hiroto
Howard, Matthew A.
Johnsrude, Ingrid S.
author_facet Billig, Alexander J.
Herrmann, Björn
Rhone, Ariane E.
Gander, Phillip E.
Nourski, Kirill V.
Snoad, Beau F.
Kovach, Christopher K.
Kawasaki, Hiroto
Howard, Matthew A.
Johnsrude, Ingrid S.
author_sort Billig, Alexander J.
collection PubMed
description The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschl's gyrus (HG) with pronounced induced high-frequency (70–150 Hz) activity and short-latency responses that phase-lock to rapid transient sounds. Low-frequency neural oscillations are also relevant to stimulus processing and information flow, however, their distribution within auditory cortex has not been established. Alpha activity (7–14 Hz) in particular has been associated with processes that may differentially engage earlier versus later levels of the cortical hierarchy, including functional inhibition and the communication of sensory predictions. These theories derive largely from the study of occipitoparietal sources readily detectable in scalp electroencephalography. To characterize the anatomical basis and functional significance of less accessible temporal-lobe alpha activity we analyzed responses to sentences in seven human adults (4 female) with epilepsy who had been implanted with electrodes in superior temporal cortex. In contrast to primary cortex in posteromedial HG, a non-primary field in anterolateral HG was characterized by high spontaneous alpha activity that was strongly suppressed during auditory stimulation. Alpha-power suppression decreased with distance from anterolateral HG throughout superior temporal cortex, and was more pronounced for clear compared to degraded speech. This suppression could not be accounted for solely by a change in the slope of the power spectrum. The differential manifestation and stimulus-sensitivity of alpha oscillations across auditory fields should be accounted for in theories of their generation and function. SIGNIFICANCE STATEMENT To understand how auditory cortex is organized in support of perception, we recorded from patients implanted with electrodes for clinical reasons. This allowed measurement of activity in brain regions at different levels of sensory processing. Oscillations in the alpha range (7–14 Hz) have been associated with functions including sensory prediction and inhibition of regions handling irrelevant information, but their distribution within auditory cortex is not known. A key finding was that these oscillations dominated in one particular non-primary field, anterolateral Heschl's gyrus, and were suppressed when subjects listened to sentences. These results build on our knowledge of the functional organization of auditory cortex and provide anatomical constraints on theories of the generation and function of alpha oscillations.
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spelling pubmed-68202042019-10-31 A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex Billig, Alexander J. Herrmann, Björn Rhone, Ariane E. Gander, Phillip E. Nourski, Kirill V. Snoad, Beau F. Kovach, Christopher K. Kawasaki, Hiroto Howard, Matthew A. Johnsrude, Ingrid S. J Neurosci Research Articles The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschl's gyrus (HG) with pronounced induced high-frequency (70–150 Hz) activity and short-latency responses that phase-lock to rapid transient sounds. Low-frequency neural oscillations are also relevant to stimulus processing and information flow, however, their distribution within auditory cortex has not been established. Alpha activity (7–14 Hz) in particular has been associated with processes that may differentially engage earlier versus later levels of the cortical hierarchy, including functional inhibition and the communication of sensory predictions. These theories derive largely from the study of occipitoparietal sources readily detectable in scalp electroencephalography. To characterize the anatomical basis and functional significance of less accessible temporal-lobe alpha activity we analyzed responses to sentences in seven human adults (4 female) with epilepsy who had been implanted with electrodes in superior temporal cortex. In contrast to primary cortex in posteromedial HG, a non-primary field in anterolateral HG was characterized by high spontaneous alpha activity that was strongly suppressed during auditory stimulation. Alpha-power suppression decreased with distance from anterolateral HG throughout superior temporal cortex, and was more pronounced for clear compared to degraded speech. This suppression could not be accounted for solely by a change in the slope of the power spectrum. The differential manifestation and stimulus-sensitivity of alpha oscillations across auditory fields should be accounted for in theories of their generation and function. SIGNIFICANCE STATEMENT To understand how auditory cortex is organized in support of perception, we recorded from patients implanted with electrodes for clinical reasons. This allowed measurement of activity in brain regions at different levels of sensory processing. Oscillations in the alpha range (7–14 Hz) have been associated with functions including sensory prediction and inhibition of regions handling irrelevant information, but their distribution within auditory cortex is not known. A key finding was that these oscillations dominated in one particular non-primary field, anterolateral Heschl's gyrus, and were suppressed when subjects listened to sentences. These results build on our knowledge of the functional organization of auditory cortex and provide anatomical constraints on theories of the generation and function of alpha oscillations. Society for Neuroscience 2019-10-30 /pmc/articles/PMC6820204/ /pubmed/31533976 http://dx.doi.org/10.1523/JNEUROSCI.0696-19.2019 Text en Copyright © 2019 Billig, Herrmann et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Billig, Alexander J.
Herrmann, Björn
Rhone, Ariane E.
Gander, Phillip E.
Nourski, Kirill V.
Snoad, Beau F.
Kovach, Christopher K.
Kawasaki, Hiroto
Howard, Matthew A.
Johnsrude, Ingrid S.
A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex
title A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex
title_full A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex
title_fullStr A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex
title_full_unstemmed A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex
title_short A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex
title_sort sound-sensitive source of alpha oscillations in human non-primary auditory cortex
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6820204/
https://www.ncbi.nlm.nih.gov/pubmed/31533976
http://dx.doi.org/10.1523/JNEUROSCI.0696-19.2019
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