The 40-Hz auditory steady-state response enhanced by beta-band subharmonics

Shunsuke Sugiyama; Tomoya Taniguchi; Tomoaki Kinukawa; Nobuyuki Takeuchi; Kazutaka Ohi; Toshiki Shioiri; Makoto Nishihara; Koji Inui

doi:10.3389/fnins.2023.1127040

The 40-Hz auditory steady-state response enhanced by beta-band subharmonics

Front Neurosci. 2023 Feb 24:17:1127040. doi: 10.3389/fnins.2023.1127040. eCollection 2023.

Authors

Shunsuke Sugiyama¹, Tomoya Taniguchi², Tomoaki Kinukawa², Nobuyuki Takeuchi³, Kazutaka Ohi¹, Toshiki Shioiri¹, Makoto Nishihara⁴, Koji Inui^{5

6}

Affiliations

¹ Department of Psychiatry, Gifu University Graduate School of Medicine, Gifu, Japan.
² Department of Anesthesiology, Nagoya University Graduate School of Medicine, Nagoya, Japan.
³ Neuropsychiatric Department, Aichi Medical University, Nagakute, Japan.
⁴ Multidisciplinary Pain Center, Aichi Medical University, Nagakute, Japan.
⁵ Department of Functioning and Disability, Institute for Developmental Research, Aichi Developmental Disability Center, Kasugai, Japan.
⁶ Section of Brain Function Information, National Institute for Physiological Sciences, Okazaki, Japan.

Abstract

The 40-Hz auditory steady-state response (ASSR) has received special attention as an index of gamma oscillations owing to its association with various neuropsychiatric disorders including schizophrenia. When a periodic stimulus is presented, oscillatory responses are often elicited not only at the stimulus frequency, but also at its harmonic frequencies. However, little is known about the effect of 40-Hz subharmonic stimuli on the activity of the 40-Hz ASSR. In the present magnetoencephalography study, we focused on the nature of oscillation harmonics and examined oscillations in a wide frequency range using a time-frequency analysis during the 6.67-, 8-, 10-, 13.3-, 20-, and 40-Hz auditory stimuli in 23 healthy subjects. The results suggested that the 40-Hz ASSR represents activation of a specific circuit tuned to this frequency. Particularly, oscillations elicited by 13.3- and 20-Hz stimuli exhibited significant enhancement at 40 Hz without changing those at the stimulus frequency. In addition, it was found that there was a non-linear response to stimulation in the beta band. We also demonstrated that the inhibition of beta to low-gamma oscillations by the 40-Hz circuit contributed to the violation of the rule that harmonic oscillations gradually decrease at higher frequencies. These findings can advance our understanding of oscillatory abnormalities in patients with schizophrenia in the future.

Keywords: auditory steady-state response; harmonic; magnetoencephalography; oscillation; schizophrenia.

Grants and funding

This study was supported by JSPS KAKENHI Grant Numbers: JP20K16624 to SS and JP18K07619 to KI and the Cooperative Study Program (22NIPS154) of the National Institute for Physiological Sciences.