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Adam T. Tierney Jennifer Krizman Nina Kraus 《Proceedings of the National Academy of Sciences of the United States of America》2015,112(32):10062-10067
Fundamental changes in brain structure and function during adolescence are well-characterized, but the extent to which experience modulates adolescent neurodevelopment is not. Musical experience provides an ideal case for examining this question because the influence of music training begun early in life is well-known. We investigated the effects of in-school music training, previously shown to enhance auditory skills, versus another in-school training program that did not focus on development of auditory skills (active control). We tested adolescents on neural responses to sound and language skills before they entered high school (pretraining) and again 3 y later. Here, we show that in-school music training begun in high school prolongs the stability of subcortical sound processing and accelerates maturation of cortical auditory responses. Although phonological processing improved in both the music training and active control groups, the enhancement was greater in adolescents who underwent music training. Thus, music training initiated as late as adolescence can enhance neural processing of sound and confer benefits for language skills. These results establish the potential for experience-driven brain plasticity during adolescence and demonstrate that in-school programs can engender these changes.By age six, the brain has reached 90% of its adult size (1). However, the years between childhood and young adulthood are marked by a host of subtler neural developments. Myelination and synaptic pruning (2–5) lead to a decrease in gray matter and an increase in white matter (6–13). Resting-state oscillations decline (14–16), and passive evoked responses to sound change in complex ways. Cortically, the P1, which is a positive deflection at around 50 ms generated within lateral Heschl’s gyrus (17), declines whereas the N1, a negative deflection at around 100 ms generated within primary and secondary auditory cortices (18–20), increases (21–23). Subcortically, the trial-by-trial consistency of the response declines (24, 25). An open question is how experience interacts with this developmental plasticity during adolescence. Is the transition from the plasticity of childhood to the stability of adulthood malleable by experience? And if so, what types of enrichment have the greatest impact on the development of the neural mechanisms contributing to auditory and language skills?Music training is an enrichment program commonly available to high school students, and its neural and behavioral consequences are well-understood (for a review, see ref. 26). Studies comparing nonmusicians with musicians who began training early in life have revealed a “signature” set of enhancements associated with musical experience (27, 28). Relative to nonmusician peers, musicians tend to show enhanced speech-in-noise perception (29–34), verbal memory (30–33, 35–38), phonological skills (39–45), and reading (46–50), although not without exception (51, 52). Music training has also been linked to enhancements in the encoding of sound throughout the auditory system. For example, musicians show an enhanced N1 (53–56). These enhancements extend to the subcortical auditory system, with musicians showing responses to sound that are faster (55, 57–61), are degraded less by background noise (32, 61), represent speech formant structure more robustly (32, 62–64). differentiate speech sounds to a greater extent (65–67), track stimulus pitch more accurately (68, 69), and are more consistent across trials (59, 70). In adolescence, music training leads to faster responses to speech in noise (71), but the extent to which adolescent music training can confer other aspects of the musician signature remains unknown.Motivated by a conceptual framework in which auditory enrichment interacts with the auditory processes that remain under development during adolescence, we undertook a school-based longitudinal study of adolescent auditory enrichment. We focused on objective biological measures of sound processing that (i) have shown developmental plasticity during adolescence in the absence of intervention and (ii) contribute to the “neural signature” of musicianship: the consistency of the subcortical response to speech and the magnitude of the cortical onset response to speech. Subcortical response consistency peaks in childhood, waning into young adulthood (24), coinciding with a period when learning a second language becomes more difficult than earlier in life (72). Response consistency tracks with language skills (73) and is enhanced in musicians (59, 70). Accordingly, we predicted that music training in adolescence prolongs this period of heightened auditory stability. Moreover, given that the cortical N1 onset response emerges during adolescence while the P1 response declines (17, 18, 21–23), and that N1 is enhanced in younger and older musicians (53–56), we predicted that music training during adolescence would accelerate the development of the cortical onset response.To test these hypotheses, we followed two groups of high school students longitudinally, testing them just before they entered high school (mean age 14.7) and again 4 y later during their last year of school. One group (n = 19) engaged in music training in which they performed music from written notation in a group setting whereas the active control group (n = 21) engaged in Junior Reserve Officers Training Corps (JROTC) training. Both types of training required investment of time and effort and emphasized the development of self-discipline, dedication, and determination; however, only the music training targeted auditory function. Both activities were part of the high school curriculum, which was otherwise identical for both groups. We also tested students’ language skills (phonological memory, phonological awareness, and rapid naming ability) to determine whether in-school music engendered benefits for literacy skills, a prediction consistent with cross-sectional studies (39–45). The two groups were matched demographically and on all outcome measures at the start of the study (see Demographic information Music training JROTC training No. female 8 8 Age at pretest 14.66 (0.42) 14.72 (0.38) Nonverbal IQ scores at pretest 51.74 (9.88) 51.14 (4.75) Avg degree of maternal education* 2.53 (0.84) 2.4 (0.75)