Chronology of auditory processing and related co-activation in the orbitofrontal cortex depends on musical expertise - PubMed (original) (raw)

Steffen Bücher et al. Front Neurosci. 2023.

Abstract

Introduction: The present study aims to explore the extent to which auditory processing is reflected in the prefrontal cortex.

Methods: Using magnetoencephalography (MEG), we investigated the chronology of primary and secondary auditory responses and associated co-activation in the orbitofrontal cortex in a large cohort of 162 participants of various ages. The sample consisted of 38 primary school children, 39 adolescents, 43 younger, and 42 middle-aged adults and was further divided into musically experienced participants and non-musicians by quantifying musical training and aptitude parameters.

Results: We observed that the co-activation in the orbitofrontal cortex [Brodmann-Area 10 (BA10)] strongly depended on musical expertise but not on age. In the musically experienced groups, a systematic coincidence of peak latencies of the primary auditory P1 response and the co-activated response in the orbitofrontal cortex was observed in childhood at the onset of musical education. In marked contrast, in all non-musicians, the orbitofrontal co-activation occurred 25-40 ms later when compared with the P1 response. Musical practice and musical aptitude contributed equally to the observed activation and co-activation patterns in the auditory and orbitofrontal cortex, confirming the reciprocal, interrelated influence of nature, and nurture in the musical brain.

Discussion: Based on the observed ageindependent differences in the chronology and lateralization of neurological responses, we suggest that orbitofrontal functions may contribute to musical learning at an early age.

Keywords: BA10; audiation; auditory cortex; auditory evoked fields; chronology; musical aptitude; orbitofrontal cortex.

Copyright © 2023 Bücher, Bernhofs, Thieme, Christiner and Schneider.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1

FIGURE 1

Musical aptitude and cumulative amount of musical training (A) group-averaged perceptual score of the IMMA/AMMA-tests, (B) group-averaged IMP values. The bold solid lines (circles) depict the values of the musicians, the dashed lines (triangles) those of the non-musicians. C, children; A, adolescents; Y, young adults; M, middle-aged adults. “Mus” represent the musicians, while “Non” illustrates the non-musicians.

FIGURE 2

FIGURE 2

Source modeling in auditory cortex and frontal lobe. (A) Top view on the left and right auditory cortex including the right (red) and left (blue) Heschl’s gyrus and the localization of the primary auditory evoked and orbitofrontally seeded responses depicted as green and pink dipoles bilaterally, respectively. (B) Source waveforms of the left and right primary activity (green) and the orbitofrontally seeded musical aesthetic activation (pink). (C) Source locations of the four dipoles projected in a spherical head model calculated with BESA software (Scherg, 1990).

FIGURE 3

FIGURE 3

Auditory evoked fields in response to instrumental and harmonic complex sounds. The superior curve shows the auditory evoked P1-N1-P2 complex followed by a sustained field and the offset about 600 ms after tone onset. The inferior curve depicts the coactivated response of the orbitofrontal cortex, seeded with fixed coordinates in the center of the BA10 region. The subpanels (A–D) show the responses of the musicians, subpanel (E–H) those of the non-musicians [(A,E) children; (B,F) adolescents; (C,G) young adults; (D,H) middle-aged adults]. Arrows indicate the first onset peak of the auditory and orbitofrontal response, respectively. Red curve, right hemisphere; dark blue curve, left hemisphere.

FIGURE 4

FIGURE 4

Age related changes of the most important MEG variables. Group averaged values of (A) P1 latency (B) P2 latency (C) P2 amplitude (D) BA10 latency (E) BA10 amplitude (F) BA10-P1 latency difference, averaged over both hemispheres, respectively. Y-axis, latencies in ms and amplitudes in nAm. X-Axis, Subgroups of children (C), adolescents (A), young adults (Y), and middle-aged adults (O). Solid lines (circles), musicians; dashed lines (triangles), non-musicians.

FIGURE 5

FIGURE 5

Correlational analyses between behavioral and MEG variables. (A,D) Represent BA10 latency and AMMA/IMMA score correlations; (B,E) BA10 latency and IMP cumulative; (C,F) BA10 latency and P2 amplitude. (A–C) Depict the correlations over all subjects, colors indicate here the four age groups. (D–F) Depict the correlations separately for the musicians (circles) and the non-musicians (crosses); n.s., non-significant.

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