Neuroanatomical Disposition, Natural Development, and Training-Induced Plasticity of the Human Auditory System from Childhood to Adulthood: A 12-Year Study in Musicians and Nonmusicians - PubMed (original) (raw)
. 2023 Sep 13;43(37):6430-6446.
doi: 10.1523/JNEUROSCI.0274-23.2023. Epub 2023 Aug 21.
Peter Schneider 1 2 3 4, Christine Groß 2 4, Valdis Bernhofs 4, Elke Hofmann 5, Markus Christiner 6 2 4, Jan Benner 3, Steffen Bücher 2, Alexander Ludwig 3, Bettina L Serrallach 2 3, Bettina M Zeidler 6 3, Sabrina Turker 7, Richard Parncutt 6, Annemarie Seither-Preisler 1 8
Affiliations
- PMID: 37604688
- PMCID: PMC10500984
- DOI: 10.1523/JNEUROSCI.0274-23.2023
Neuroanatomical Disposition, Natural Development, and Training-Induced Plasticity of the Human Auditory System from Childhood to Adulthood: A 12-Year Study in Musicians and Nonmusicians
Peter Schneider et al. J Neurosci. 2023.
Abstract
Auditory perception is fundamental to human development and communication. However, no long-term studies have been performed on the plasticity of the auditory system as a function of musical training from childhood to adulthood. The long-term interplay between developmental and training-induced neuroplasticity of auditory processing is still unknown. We present results from AMseL (Audio and Neuroplasticity of Musical Learning), the first longitudinal study on the development of the human auditory system from primary school age until late adolescence. This 12-year project combined neurologic and behavioral methods including structural magnetic resonance imaging (MRI), magnetoencephalography (MEG), and auditory tests. A cohort of 112 typically developing participants (51 male, 61 female), classified as "musicians" (n = 66) and "nonmusicians" (n = 46), was tested at five measurement timepoints. We found substantial, stable differences in the morphology of auditory cortex (AC) between musicians and nonmusicians even at the earliest ages, suggesting that musical aptitude is manifested in macroscopic neuroanatomical characteristics. Maturational plasticity led to a continuous increase in white matter myelination and systematic changes of the auditory evoked P1-N1-P2 complex (decreasing latencies, synchronization effects between hemispheres, and amplitude changes) regardless of musical expertise. Musicians showed substantial training-related changes at the neurofunctional level, in particular more synchronized P1 responses and bilaterally larger P2 amplitudes. Musical training had a positive influence on elementary auditory perception (frequency, tone duration, onset ramp) and pattern recognition (rhythm, subjective pitch). The observed interplay between "nature" (stable biological dispositions and natural maturation) and "nurture" (learning-induced plasticity) is integrated into a novel neurodevelopmental model of the human auditory system.Significance Statement We present results from AMseL (Audio and Neuroplasticity of Musical Learning), a 12-year longitudinal study on the development of the human auditory system from childhood to adulthood that combined structural magnetic resonance imaging (MRI), magnetoencephalography (MEG), and auditory discrimination and pattern recognition tests. A total of 66 musicians and 46 nonmusicians were tested at five timepoints. Substantial, stable differences in the morphology of auditory cortex (AC) were found between the two groups even at the earliest ages, suggesting that musical aptitude is manifested in macroscopic neuroanatomical characteristics. We also observed neuroplastic and perceptual changes with age and musical practice. This interplay between "nature" (stable biological dispositions and natural maturation) and "nurture" (learning-induced plasticity) is integrated into a novel neurodevelopmental model of the human auditory system.
Keywords: auditory cortex; auditory evoked fields; learning-induced plasticity; maturation; morphology; musical practice.
Copyright © 2023 the authors.
Figures
Figure 1.
Group-specific differences in musical practice and musical aptitude. A, Longitudinal indices of musical practice (IMPs) of the musician and nonmusician groups (8–18 years) along with cross-sectional IMPs of adult young and middle-aged adult nonmusicians and musicians (YA: 19-29 years; MA: 30-67 years). B, Correlation of the total score of the musical aptitude test AMMA (Gordon, 1989), including both the tonal and rhythmic dimension, with musical experience (IMP4).
Figure 2.
Structural development of human auditory cortex (AC). Gray and white matter (GW) distributions for (A) Heschl’s gyrus (HG) and (B) Planum temporale (PT) in the right (red) and left (blue) hemisphere. Gray matter (GM) volumes (C, D) and white and gray matter (WG) ratios (E, F) of right (red) and left (blue) HG (bold lines) and PT (dashed lines); GM value range: 0 (dark gray) to 225 (white). Data are shown for musically trained (C, E) and untrained (D, F) individuals at five measurement timepoints (MT) from childhood to late adolescence. In addition, data from young (YA) and middle-aged (MA) adults from previous cross-sectionals studies are displayed. Error bars: SEM.
Figure 3.
Development of auditory evoked fields in the lifetime perspective. A, Three-dimensional reconstruction of right and left auditory cortex (AC) of a child. B, Two-dipole model to extract the individual source waveforms (activation over time) in the regions of left (blue) and right (red) AC. C, D, Averaged source waveforms of musicians (left column) and nonmusicians (right column) and their longitudinal changes from childhood to late adolescence. The graph is complemented by data from previous cross-sectional studies with young (YA) and middle-aged (MA) adults (MA). Maturational plasticity led to continuously decreasing latencies of all auditory evoked responses, synchronization of P1 and N1 between the hemispheres, a decrease in P1 amplitude and an increase in N1 and P2 amplitudes, regardless of musical expertise. Latencies decreased systematically from MT1 to MT5. For each of the three considered auditory evoked field (AEF) components, latencies were significantly shorter in the right hemisphere. Moreover, the latencies of the P1 and P2 decreased faster over time in the right than in the left hemisphere. While for the N1 and P2 this right lead was observed throughout the observation period, it was significant for the P1 component only up to an age of ∼12 years. The N1 becomes clearly visible at an age of 11–12 years (MT3) and then further increases. Data from young and middle-aged adults (YA, MA) reveal in addition that this process continues throughout life (C, D, bottom). The P2 response first becomes evident in mid-adolescence (MT3–4) and continues to increase into adulthood. In this way, our comprehensive longitudinal data demonstrate for the first time that the biological development of the human AC progresses throughout life.
Figure 4.
Long-term improvement of auditory perception. Discrimination abilities of musicians and nonmusicians for (A) frequency, (B) intensity, (C) onset ramp, (D) tone duration, and (E) rhythm. F, Subjective pitch perception of harmonic complex tones. The five follow-up measurement timepoints (MT) from childhood to late adolescence are displayed by connected circles. Graphs are complemented by data from previous cross-sectional studies with young (YA) and middle-aged (MA) adults. Musical training had a positive influence on almost all dimensions of auditory perception (A, C–F) except intensity (B). All assessed auditory skills significantly improved over time. The discrimination of tone duration (D) and rhythm perception (E) did not further improve in adolescence. The development of subjective pitch perception (F) reveals clear plastic changes until adulthood, which is reflected in a U-shaped curve. Three distinct developmental stages can be inferred from the relative predominance of fundamental over spectral pitch sensations (see Materials and Methods): (1) in early childhood, the global spectral sensation of timbre appears to represent the primary mode of sound perception, which is then (2) gradually overridden toward late adolescence by the more abstract ability to extract the fundamental frequency of harmonic complex sounds. (3) Even later, the analytical ability to pick out individual harmonics from a given spectrum emerges, shifting the curve back to the spectral dimension. This reflects a progressive cognitive flexibility with age in terms of auditory pattern recognition and feature extraction, with levels of analysis that are not mutually exclusive but rather complementary.
Figure 5.
Correlational findings. A, Correlation of the tonal AMMA score with right GM volume; correlation of the total AMMA score with (B) left N1 amplitude, (C) pitch perception preference (ppp) index, (D) frequency discrimination threshold, (E) duration threshold. F, Correlation of “absolute P1 asynchrony” with the social variable “education environment.”
Figure 6.
Integrative neurodevelopmental model of the auditory system. Interplay of perceptual and neuroanatomical dispositions (peripheral and cortical; bottom), maturational (left) and learning-induced (right) plasticity for shaping individual listening competence (top). The former two represent the aspects of “nature,” the latter the aspect of “nurture.” The high interindividual variability and intraindividual stability of HG and PT gray matter volumes (gray circle, bottom left) suggest that these are neuroanatomical markers of “musical aptitude.” The maturational plasticity of AC (left path, blue circle) is reflected not only structurally in the degree of myelination, but also functionally in decreasing latencies and varying amplitudes of the P1-N1-P2 complex, and in the bilateral synchronization of P1 and N1. Moreover, musical training resulted in substantial learning-induced changes at the neurofunctional level (right path, red circle). Evidently, individual neuroanatomical dispositions of AC have a major impact on musical learning behavior, which in turn at the neurofunctional level enhances the efficiency of the involved structures. This training-induced plasticity leads to a continuous refinement of sound perception abilities. Together with natural biological maturation that applies equally to musically trained and untrained participants, it provides the framework for an even more efficient auditory processing, and thus for individual listening competence (white circle, top). The latter is also crucial for sensorimotor integration and further transfer effects into cognitive domains, such as language, literacy, and attentional skills.
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