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

• Published in: The Journal of neuroscience Vol. 39; no. 44; pp. 8679 - 8689
• Main Authors: Billig, Alexander J, Herrmann, Björn, Rhone, Ariane E, Gander, Phillip E, Nourski, Kirill V, Snoad, Beau F, Kovach, Christopher K, Kawasaki, Hiroto, Howard, 3rd, Matthew A, Johnsrude, Ingrid S
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 30.10.2019
• Subjects: Acoustic Stimulation; Acoustics; Adult; Alpha Rhythm; Auditory Cortex - physiology; Auditory Pathways - physiology; Cortex (auditory); Cortex (somatosensory); Cortex (temporal); EEG; Electroencephalography; Epilepsy; Evoked Potentials, Auditory; Female; Functional morphology; Gamma Rhythm; Hearing; Humans; Information flow; Information processing; Latency; Male; Middle Aged; Oscillations; Scalp; Sensory stimulation; Speech Perception - physiology; Temporal Lobe - physiology; Young Adult; intracranial; auditory cortex; functional inhibition; high gamma; speech; alpha
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.0696-19.2019

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. 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.