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

• Published in: Hearing research Vol. 449; p. 109032
• Main Authors: Yusuf, Prasandhya A., Hubka, Peter, Konerding, Wiebke, Land, Rüdiger, Tillein, Jochen, Kral, Andrej
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.08.2024
• Subjects: Acoustic Stimulation; Algorithms; Alpha band; Alpha Rhythm; Animals; Auditory Cortex - physiopathology; Auditory Pathways - physiopathology; Cats; Cochlear implant; Cochlear Implants; Connectivity; Deafness - congenital; Deafness - physiopathology; Development; Disease Models, Animal; Evoked Potentials, Auditory; Gamma Rhythm; Hearing loss; Theta band; Theta Rhythm; Alpha band; Cochlear implant; Development; Theta band; Connectivity; Hearing loss
• ISSN: 0378-5955; 1878-5891; 1878-5891
• DOI: 10.1016/j.heares.2024.109032

•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. 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.