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A sound-sensitive source of alpha oscillations in human non-primary auditory cortex.
J Neurosci 2019JN

Abstract

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 (four 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 STATEMENTTo 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.

Authors+Show Affiliations

The Brain and Mind Institute, University of Western Ontario, London, ON, N6A 3K7, Canada ajbillig@gmail.com.The Brain and Mind Institute, University of Western Ontario, London, ON, N6A 3K7, Canada.Department of Neurosurgery, The University of Iowa, Iowa City, IA, 52242, USA.Department of Neurosurgery, The University of Iowa, Iowa City, IA, 52242, USA.Department of Neurosurgery, The University of Iowa, Iowa City, IA, 52242, USA. Iowa Neuroscience Institute, The University of Iowa, Iowa City, IA, 52242, USA.Department of Neurosurgery, The University of Iowa, Iowa City, IA, 52242, USA.Department of Neurosurgery, The University of Iowa, Iowa City, IA, 52242, USA.Department of Neurosurgery, The University of Iowa, Iowa City, IA, 52242, USA.Department of Neurosurgery, The University of Iowa, Iowa City, IA, 52242, USA. Iowa Neuroscience Institute, The University of Iowa, Iowa City, IA, 52242, USA. Pappajohn Biomedical Institute, The University of Iowa, Iowa City, IA, 52242, USA.The Brain and Mind Institute, University of Western Ontario, London, ON, N6A 3K7, Canada. School of Communication Sciences and Disorders, University of Western Ontario, London, ON, N6A 5B7, Canada.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31533976

Citation

Billig, Alexander J., et al. "A Sound-sensitive Source of Alpha Oscillations in Human Non-primary Auditory Cortex." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 2019.
Billig AJ, Herrmann B, Rhone AE, et al. A sound-sensitive source of alpha oscillations in human non-primary auditory cortex. J Neurosci. 2019.
Billig, A. J., Herrmann, B., Rhone, A. E., Gander, P. E., Nourski, K. V., Snoad, B. F., ... Johnsrude, I. S. (2019). A sound-sensitive source of alpha oscillations in human non-primary auditory cortex. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, doi:10.1523/JNEUROSCI.0696-19.2019.
Billig AJ, et al. A Sound-sensitive Source of Alpha Oscillations in Human Non-primary Auditory Cortex. J Neurosci. 2019 Sep 18; PubMed PMID: 31533976.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A sound-sensitive source of alpha oscillations in human non-primary auditory cortex. AU - Billig,Alexander J, AU - Herrmann,Björn, AU - Rhone,Ariane E, AU - Gander,Phillip E, AU - Nourski,Kirill V, AU - Snoad,Beau F, AU - Kovach,Christopher K, AU - Kawasaki,Hiroto, AU - Howard,Matthew A,3rd AU - Johnsrude,Ingrid S, Y1 - 2019/09/18/ PY - 2019/03/27/received PY - 2019/06/09/revised PY - 2019/07/02/accepted PY - 2019/9/20/entrez PY - 2019/9/20/pubmed PY - 2019/9/20/medline JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. N2 - 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 (four 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 STATEMENTTo 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. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/31533976/A_sound-sensitive_source_of_alpha_oscillations_in_human_non-primary_auditory_cortex L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=31533976 DB - PRIME DP - Unbound Medicine ER -