Intracranial electrophysiology of spectrally degraded speech in the human cortex
IntroductionCochlear implants (CIs) are the treatment of choice for severe to profound hearing loss. Variability in CI outcomes remains despite advances in technology and is attributed in part to differences in cortical processing. Studying these differences in CI users is technically challenging. S...
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Human Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1334742/full |
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| author | Kirill V. Nourski Kirill V. Nourski Mitchell Steinschneider Mitchell Steinschneider Ariane E. Rhone Joel I. Berger Emily R. Dappen Emily R. Dappen Hiroto Kawasaki Matthew A. Howard III Matthew A. Howard III Matthew A. Howard III |
| author_facet | Kirill V. Nourski Kirill V. Nourski Mitchell Steinschneider Mitchell Steinschneider Ariane E. Rhone Joel I. Berger Emily R. Dappen Emily R. Dappen Hiroto Kawasaki Matthew A. Howard III Matthew A. Howard III Matthew A. Howard III |
| author_sort | Kirill V. Nourski |
| collection | DOAJ |
| description | IntroductionCochlear implants (CIs) are the treatment of choice for severe to profound hearing loss. Variability in CI outcomes remains despite advances in technology and is attributed in part to differences in cortical processing. Studying these differences in CI users is technically challenging. Spectrally degraded stimuli presented to normal-hearing individuals approximate input to the central auditory system in CI users. This study used intracranial electroencephalography (iEEG) to investigate cortical processing of spectrally degraded speech.MethodsParticipants were adult neurosurgical epilepsy patients. Stimuli were utterances /aba/ and /ada/, spectrally degraded using a noise vocoder (1–4 bands) or presented without vocoding. The stimuli were presented in a two-alternative forced choice task. Cortical activity was recorded using depth and subdural iEEG electrodes. Electrode coverage included auditory core in posteromedial Heschl’s gyrus (HGPM), superior temporal gyrus (STG), ventral and dorsal auditory-related areas, and prefrontal and sensorimotor cortex. Analysis focused on high gamma (70–150 Hz) power augmentation and alpha (8–14 Hz) suppression.ResultsChance task performance occurred with 1–2 spectral bands and was near-ceiling for clear stimuli. Performance was variable with 3–4 bands, permitting identification of good and poor performers. There was no relationship between task performance and participants demographic, audiometric, neuropsychological, or clinical profiles. Several response patterns were identified based on magnitude and differences between stimulus conditions. HGPM responded strongly to all stimuli. A preference for clear speech emerged within non-core auditory cortex. Good performers typically had strong responses to all stimuli along the dorsal stream, including posterior STG, supramarginal, and precentral gyrus; a minority of sites in STG and supramarginal gyrus had a preference for vocoded stimuli. In poor performers, responses were typically restricted to clear speech. Alpha suppression was more pronounced in good performers. In contrast, poor performers exhibited a greater involvement of posterior middle temporal gyrus when listening to clear speech.DiscussionResponses to noise-vocoded speech provide insights into potential factors underlying CI outcome variability. The results emphasize differences in the balance of neural processing along the dorsal and ventral stream between good and poor performers, identify specific cortical regions that may have diagnostic and prognostic utility, and suggest potential targets for neuromodulation-based CI rehabilitation strategies. |
| first_indexed | 2024-03-08T12:24:25Z |
| format | Article |
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| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-03-08T12:24:25Z |
| publishDate | 2024-01-01 |
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| series | Frontiers in Human Neuroscience |
| spelling | doaj.art-ac77467e3fdc44aa95a223ee85d159552024-01-22T10:47:59ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612024-01-011710.3389/fnhum.2023.13347421334742Intracranial electrophysiology of spectrally degraded speech in the human cortexKirill V. Nourski0Kirill V. Nourski1Mitchell Steinschneider2Mitchell Steinschneider3Ariane E. Rhone4Joel I. Berger5Emily R. Dappen6Emily R. Dappen7Hiroto Kawasaki8Matthew A. Howard III9Matthew A. Howard III10Matthew A. Howard III11Department of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesIowa Neuroscience Institute, The University of Iowa, Iowa City, IA, United StatesDepartment of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesDepartments of Neurology and Neuroscience, Albert Einstein College of Medicine, Bronx, NY, United StatesDepartment of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesDepartment of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesDepartment of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesIowa Neuroscience Institute, The University of Iowa, Iowa City, IA, United StatesDepartment of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesDepartment of Neurosurgery, The University of Iowa, Iowa City, IA, United StatesIowa Neuroscience Institute, The University of Iowa, Iowa City, IA, United StatesPappajohn Biomedical Institute, The University of Iowa, Iowa City, IA, United StatesIntroductionCochlear implants (CIs) are the treatment of choice for severe to profound hearing loss. Variability in CI outcomes remains despite advances in technology and is attributed in part to differences in cortical processing. Studying these differences in CI users is technically challenging. Spectrally degraded stimuli presented to normal-hearing individuals approximate input to the central auditory system in CI users. This study used intracranial electroencephalography (iEEG) to investigate cortical processing of spectrally degraded speech.MethodsParticipants were adult neurosurgical epilepsy patients. Stimuli were utterances /aba/ and /ada/, spectrally degraded using a noise vocoder (1–4 bands) or presented without vocoding. The stimuli were presented in a two-alternative forced choice task. Cortical activity was recorded using depth and subdural iEEG electrodes. Electrode coverage included auditory core in posteromedial Heschl’s gyrus (HGPM), superior temporal gyrus (STG), ventral and dorsal auditory-related areas, and prefrontal and sensorimotor cortex. Analysis focused on high gamma (70–150 Hz) power augmentation and alpha (8–14 Hz) suppression.ResultsChance task performance occurred with 1–2 spectral bands and was near-ceiling for clear stimuli. Performance was variable with 3–4 bands, permitting identification of good and poor performers. There was no relationship between task performance and participants demographic, audiometric, neuropsychological, or clinical profiles. Several response patterns were identified based on magnitude and differences between stimulus conditions. HGPM responded strongly to all stimuli. A preference for clear speech emerged within non-core auditory cortex. Good performers typically had strong responses to all stimuli along the dorsal stream, including posterior STG, supramarginal, and precentral gyrus; a minority of sites in STG and supramarginal gyrus had a preference for vocoded stimuli. In poor performers, responses were typically restricted to clear speech. Alpha suppression was more pronounced in good performers. In contrast, poor performers exhibited a greater involvement of posterior middle temporal gyrus when listening to clear speech.DiscussionResponses to noise-vocoded speech provide insights into potential factors underlying CI outcome variability. The results emphasize differences in the balance of neural processing along the dorsal and ventral stream between good and poor performers, identify specific cortical regions that may have diagnostic and prognostic utility, and suggest potential targets for neuromodulation-based CI rehabilitation strategies.https://www.frontiersin.org/articles/10.3389/fnhum.2023.1334742/fullauditory cortexcochlear implantsdorsal auditory streamhigh gammaiEEGnoise vocoder |
| spellingShingle | Kirill V. Nourski Kirill V. Nourski Mitchell Steinschneider Mitchell Steinschneider Ariane E. Rhone Joel I. Berger Emily R. Dappen Emily R. Dappen Hiroto Kawasaki Matthew A. Howard III Matthew A. Howard III Matthew A. Howard III Intracranial electrophysiology of spectrally degraded speech in the human cortex Frontiers in Human Neuroscience auditory cortex cochlear implants dorsal auditory stream high gamma iEEG noise vocoder |
| title | Intracranial electrophysiology of spectrally degraded speech in the human cortex |
| title_full | Intracranial electrophysiology of spectrally degraded speech in the human cortex |
| title_fullStr | Intracranial electrophysiology of spectrally degraded speech in the human cortex |
| title_full_unstemmed | Intracranial electrophysiology of spectrally degraded speech in the human cortex |
| title_short | Intracranial electrophysiology of spectrally degraded speech in the human cortex |
| title_sort | intracranial electrophysiology of spectrally degraded speech in the human cortex |
| topic | auditory cortex cochlear implants dorsal auditory stream high gamma iEEG noise vocoder |
| url | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1334742/full |
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