Insights into epileptic aphasia: Intracranial recordings in a child with a left insular ganglioglioma

\ua9 2024 The Authors. Intracranial EEG was recorded during a dialog-based task in a 16-year-old boy with a left insular ganglioglioma, medically intractable epilepsy, epileptic foci in auditory cortex on the lateral superior temporal gyrus (STG) and language deficiencies. Performance of the task was highly erratic, characterized by rapid cycling between providing correct answers, incorrect answers and failure to respond. There was no relationship between performance and the degree of concurrent epileptic activity in auditory cortex. High gamma activity in core auditory cortex (posterior medial Heschl\u27s gyrus, HGPM) was markedly diminished during listening and, with two exceptions, was less than activity from 17 control subjects. The two exceptions also had seizure onset zones in perisylvian cortex. Responses during listening were of smaller amplitude than those occurring during speaking, a pattern opposite that typically seen in the left HGPM. Within HGPM, lateral STG and pars opercularis of the inferior frontal gyrus, high gamma activity while listening was greatest when questions were correctly answered and least when the subject failed to respond. Alpha activity preceding utterances was lowest in pars opercularis when the subject failed to respond. Comparisons between resting state activity in another cohort of controls and the subject were most disparate in HGPM. Alpha activity during performance of the task was greatest in the mid-anterior cingulate when the subject failed to respond, suggesting dysfunction beyond the speech network and into the salience network. Multiple abnormalities noted in this patient paralleled those seen in epileptic aphasia and Rolandic epilepsy

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 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

Author Correction: Immediate neural impact and incomplete compensation after semantic hub disconnection (Nature Communications, (2023), 14, 1, (6264), 10.1038/s41467-023-42088-7)

\ua9 2023, The Author(s).Correction to: Nature Communications, published online 07 October 2023 In this article Thomas E. Cope, Timothy D. Griffiths, Matthew A. Howard III and Christopher I. Petkov should have been denoted as equally contributing joint senior authors. The original article has been corrected