The age-related changes in 40 Hz Auditory Steady-State Response and sustained Event-Related Fields to the same amplitude-modulated tones in typically developing children: A magnetoencephalography study

Abstract

Recent studies have revealed that gamma-band oscillatory and transient evoked potentials may change with age during childhood. It is hypothesized that these changes can be associated with a maturation of GABAergic neurotransmission and, subsequently, the age-related changes of excitation-inhibition balance in the neural circuits. One of the reliable paradigms for investigating these effects in the auditory cortex is 40 Hz Auditory Steady-State Response (ASSR), where participants are presented with the periodic auditory stimuli. It is known that such stimuli evoke two types of responses in magnetoencephalography (MEG)-40 Hz steady-state gamma response (or 40 Hz ASSR) and auditory evoked response called sustained Event-Related Field (ERF). Although several studies have been conducted in children, focusing on the changes of 40 Hz ASSR with age, almost nothing is known about the age-related changes of the sustained ERF to the same periodic stimuli and their relationships with changes in the gamma strength. Using MEG, we investigated the association between 40 Hz steady-state gamma response and sustained ERF response to the same stimuli and also their age-related changes in the group of 30 typically developing 7-to-12-year-old children. The results revealed a tight relationship between 40 Hz ASSR and ERF, indicating that the age-related increase in strength of 40 Hz ASSR was associated with the age-related decrease of the amplitude of ERF. These effects were discussed in the light of the maturation of the GABAergic system and excitation-inhibition balance development, which may contribute to the changes in ASSR and ERF.

Keywords: 40 Hz Auditory Steady-State Response; age-related changes; amplitude-modulated tones; auditory gamma oscillations; children; magnetoencephalography (MEG); sustained Event-Related Fields.

FIGURE 1

Stimulus presentation: (a) the structure of a trial; (b) pure tone with 40 Hz amplitude modulation (the duration is 1000 ms); (c) the first 70 ms of the amplitude‐modulated tone (for visualization purpose)

FIGURE 2

The grand average sensor‐space visualization: (a) “butterfly” plot; the black lines correspond to the first two obligatory transient auditory components (M50 and M100) and sustained part of ERF; the top panel shows the distribution of activity across the cortex at these timepoints; (b) time‐frequency maps of the pairs of gradiometers over the left and right temporal regions with the highest 40 Hz Inter‐Trial Phase Consistency

FIGURE 3

The localization of 40 Hz Auditory Steady‐State Response (ASSR) in MNI space: (a) grand average MNI coordinates of 40 Hz ASSR in axial, coronal, and sagittal directions; (b) MNI coordinates of 40 Hz ASSR in the left and right hemispheres: Blue dots represent the individual MNI coordinates of each child, red dots represent the grand average MNI coordinates.

FIGURE 4

The 40 Hz Auditory Steady‐State Response (ASSR) mapping, grand average: (a) time‐frequency maps for the left and right auditory regions of interests (ROIs) (normalized Inter‐Trial Phase Consistency, % change from the baseline); (b) distribution of 40 Hz ASSR across the cortex in the left and right hemispheres averaged in a 200–900 ms time interval; (c) 40 Hz steady‐state gamma synchronization during auditory stimulation (0–1050 ms); neurological convention. The amplitude threshold is set to 70% of the highest values for graphical purposes in (b) and (c).

FIGURE 5

Normalized 40 Hz intertrial phase consistency (ITPC) in the left and right auditory regions of interests (ROIs). The dots represent the individual results of each child.

FIGURE 6

The relationship between 40 Hz Auditory Steady‐State Response (ASSR) and the amplitude of the sustained part of Event‐Related Fields: (a) grand average time‐courses of the estimated sources in the left and right auditory ROIs (amplitude, z‐score). The shaded area corresponds to standard error of the mean; (b) the association between 40 Hz Inter‐Trial Phase Consistency (ITPC) and the source amplitude in the left and right hemispheres

FIGURE 7

The association between children's age and auditory responses (40 Hz Inter‐Trial Phase Consistency and the amplitude of Event‐Related Field) in the left and right auditory regions of interests (ROIs)