Gamma Activation and Alpha Suppression within Human Auditory Cortex during a Speech Classification Task

• Published in: The Journal of neuroscience Vol. 42; no. 25; pp. 5034 - 5046
• Main Authors: Nourski, Kirill V, Steinschneider, Mitchell, Rhone, Ariane E, Kovach, Christopher K, Kawasaki, Hiroto, Howard, 3rd, Matthew A
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 22.06.2022
• Subjects: Acoustic Stimulation; Auditory Cortex - physiology; Auditory Perception - physiology; Brain Mapping - methods; Classification; Cortex (auditory); Cortex (temporal); Female; Hearing; Hemispheric laterality; Humans; Information flow; Information processing; Latency; Magnetic Resonance Imaging; Male; Neurosurgery; Plains; Planum temporale; Semantics; Speech; Speech Perception - physiology; Speech processing; Superior temporal gyrus; Temporal gyrus; Words (language); electrocorticography; Heschl's gyrus; insula; superior temporal plane; iEEG; superior temporal gyrus
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.2187-21.2022

The dynamics of information flow within the auditory cortical hierarchy associated with speech processing and the emergence of hemispheric specialization remain incompletely understood. To study these questions with high spatiotemporal resolution, intracranial recordings in 29 human neurosurgical patients of both sexes were obtained while subjects performed a semantic classification task. Neural activity was recorded from posteromedial portion of Heschl's gyrus (HGPM) and anterolateral portion of Heschl's gyrus (HGAL), planum temporale (PT), planum polare, insula, and superior temporal gyrus (STG). Responses to monosyllabic words exhibited early gamma power increases and a later suppression of alpha power, envisioned to represent feedforward activity and decreased feedback signaling, respectively. Gamma activation and alpha suppression had distinct magnitude and latency profiles. HGPM and PT had the strongest gamma responses with shortest onset latencies, indicating that they are the earliest auditory cortical processing stages. The origin of attenuated top-down influences in auditory cortex, as indexed by alpha suppression, was in STG and HGAL. Gamma responses and alpha suppression were typically larger to nontarget words than tones. Alpha suppression was uniformly greater to target versus nontarget stimuli. Hemispheric bias for words versus tones and for target versus nontarget words, when present, was left lateralized. Better task performance was associated with increased gamma activity in the left PT and greater alpha suppression in HGPM and HGAL bilaterally. The prominence of alpha suppression during semantic classification and its accessibility for noninvasive electrophysiologic studies suggests that this measure is a promising index of auditory cortical speech processing. Understanding the dynamics of cortical speech processing requires the use of active tasks. This is the first comprehensive intracranial electroencephalography study to examine cortical activity within the superior temporal plane, lateral superior temporal gyrus, and the insula during a semantic classification task. Distinct gamma activation and alpha suppression profiles clarify the functional organization of feedforward and feedback processing within the auditory cortical hierarchy. Asymmetries in cortical speech processing emerge at early processing stages. Relationships between cortical activity and task performance are interpreted in the context of current models of speech processing. Results lay the groundwork for iEEG studies using connectivity measures of the bidirectional information flow within the auditory processing hierarchy.