Congenital deafness reduces alpha-gamma cross-frequency coupling in the auditory cortex

  • Highlights • Reduced evoked theta activity in the deaf. • Reduced theta-gamma and alpha-gamma cross-frequency couplings in the deaf. • Stronger delta-alpha coupling in the deaf. Abstract Neurons within a neuronal network can be grouped by bottom-up and top-down influences using synchrony in neuronal oscillations. This creates the representation of perceptual objects from sensory features. Oscillatory activity can be differentiated into stimulus-phase-locked (evoked) and non-phase-locked (induced). The former is mainly determined by sensory input, the latter by higher-level (cortical) processing. Effects of auditory deprivation on cortical oscillations have been studied in congenitally deaf cats (CDCs) using cochlear implant (CI) stimulation. CI-induced alpha, beta, and gamma activity were compromised in the auditory cortex of CDCs. Furthermore, top-down information flow between secondary and primary auditory areas in hearing cats, conveyed by induced alpha oscillations, was lost in CDCs. Here we used the matching pursuit algorithm to assess components of such oscillatory activity in local field potentials recorded in primary field A1. Additionally to the loss of induced alpha oscillations, we also found a loss of evoked theta activity in CDCs. The loss of theta and alpha activity in CDCs can be directly related to reduced high-frequency (gamma-band) activity due to cross-frequency coupling. Here we quantified such cross-frequency coupling in adult 1) hearing-experienced, acoustically stimulated cats (aHCs), 2) hearing-experienced cats following acute pharmacological deafening and subsequent CIs, thus in electrically stimulated cats (eHCs), and 3) electrically stimulated CDCs. We found significant cross-frequency coupling in all animal groups in > 70% of auditory-responsive sites. The predominant coupling in aHCs and eHCs was between theta/alpha phase and gamma power. In CDCs such coupling was lost and replaced by alpha oscillations coupling to delta/theta phase. Thus, alpha/theta oscillations synchronize high-frequency gamma activity only in hearing-experienced cats. The absence of induced alpha and theta oscillations contributes to the loss of induced gamma power in CDCs, thereby signifying impaired local network activity.

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Metadaten
Author:Prasandhya Astagiri YusufORCiDGND, Peter HubkaORCiD, Wiebke KonerdingORCiD, Rüdiger LandORCiDGND, Jochen TilleinORCiD, Andrej KralORCiDGND
URN:urn:nbn:de:hebis:30:3-855135
DOI:https://doi.org/10.1016/j.heares.2024.109032
ISSN:0378-5955
Parent Title (English):Hearing research
Publisher:Elsevier
Place of publication:Amsterdam
Document Type:Article
Language:English
Date of Publication (online):2024/07/25
Date of first Publication:2024/05/17
Publishing Institution:Universitätsbibliothek Johann Christian Senckenberg
Release Date:2024/07/18
Tag:Cochlear implant; alpha band; connectivity; development; hearing loss; theta band
Volume:449
Issue:109032
Article Number:109032
Page Number:12
HeBIS-PPN:52086901X
Institutes:Medizin
Dewey Decimal Classification:6 Technik, Medizin, angewandte Wissenschaften / 61 Medizin und Gesundheit / 610 Medizin und Gesundheit
Sammlungen:Universitätspublikationen
Licence (German):License LogoCreative Commons - CC BY-NC-ND - Namensnennung - Nicht kommerziell - Keine Bearbeitungen 4.0 International