Music training alters the course of adolescent auditory development

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 32, 2015, Pages 10062-10067

  Tierney, Adam T ^a,d   Krizman, Jennifer ^a   Kraus, Nina ^a,b   Tallal, Paula ^c  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Auditory; Music; Training

Indexed keywords

ADOLESCENCE; ADOLESCENT; ARTICLE; AUDITORY DISCRIMINATION; AUDITORY RESPONSE; CONTROLLED STUDY; FEMALE; HEARING; HIGH SCHOOL; HUMAN; HUMAN EXPERIMENT; LANGUAGE; MALE; MUSIC; NERVE CELL PLASTICITY; NERVE POTENTIAL; NORMAL HUMAN; PHONETICS; PRIORITY JOURNAL; SKILL; SOUND; TRAINING; AUDITORY CORTEX; BEHAVIOR; DEMOGRAPHY; ELECTRODE; GROWTH, DEVELOPMENT AND AGING; MEMORY; PHYSIOLOGY;

ADOLESCENT; AUDITORY CORTEX; AUDITORY PERCEPTION; BEHAVIOR; DEMOGRAPHY; ELECTRODES; FEMALE; HUMANS; MALE; MEMORY; MUSIC; PHONETICS;

EID: 84938948214     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505114112     Document Type: Article

References (99)

1. Giedd JN (2004) Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 1021: 77-85.
2. Huttenlocher PR (1979) Synaptic density in human frontal cortex: Developmental changes and effects of aging. Brain Res 163(2): 195-205.
3. Huttenlocher PR (1990) Morphometric study of human cerebral cortex development. Neuropsychologia 28(6): 517-527.
4. Huttenlocher PR, Dabholkar AS (1997) Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387(2): 167-178.
5. Paus T, et al. (1999) Structural maturation of neural pathways in children and adolescents: In vivo study. Science 283(5409): 1908-1911.
6. Pfefferbaum A, et al. (1994) A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch Neurol 51(9): 874-887.
7. Reiss AL, Abrams MT, Singer HS, Ross JL, Denckla MB (1996) Brain development, gender and IQ in children: A volumetric imaging study. Brain 119(Pt 5): 1763-1774.
8. Sowell ER, et al. (1999) Localizing age-related changes in brain structure between childhood and adolescence using statistical parametric mapping. Neuroimage 9(6 Pt 1): 587-597.
9. Sowell ER, Thompson PM, Tessner KD, Toga AW (2001) Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: Inverse relationships during postadolescent brain maturation. J Neurosci 21(22): 8819-8829.
10. Sowell ER, et al. (2003) Mapping cortical change across the human life span. Nat Neurosci 6(3): 309-315.
11. Giedd JN, et al. (1999) Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2(10): 861-863.
12. Courchesne E, et al. (2000) Normal brain development and aging: Quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 216(3): 672-682.
13. Gogtay N, et al. (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101(21): 8174-8179.
14. Benninger C, Matthis P, Scheffner D (1984) EEG development of healthy boys and girls: Results of a longitudinal study. Electroencephalogr Clin Neurophysiol 57(1): 1-12.
15. Clarke AR, Barry RJ, McCarthy R, Selikowitz M (2001) Age and sex effects in the EEG: Development of the normal child. Clin Neurophysiol 112(5): 806-814.
16. Campbell IG, Feinberg I (2009) Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. Proc Natl Acad Sci USA 106(13): 5177-5180.
17. Liégeois-Chauvel C, Musolino A, Badier JM, Marquis P, Chauvel P (1994) Evoked potentials recorded from the auditory cortex in man: Evaluation and topography of the middle latency components. Electroencephalogr Clin Neurophysiol 92(3): 204-214.
18. Näätänen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: A review and an analysis of the component structure. Psychophysiology 24(4): 375-425.
19. Woods DL (1995) The component structure of the N1 wave of the human auditory evoked potential. Electroencephalogr Clin Neurophysiol 44(Suppl): 102-109.
20. Godey B, Schwartz D, de Graaf JB, Chauvel P, Liégeois-Chauvel C (2001) Neuromagnetic source localization of auditory evoked fields and intracerebral evoked potentials: A comparison of data in the same patients. Clin Neurophysiol 112(10): 1850-1859.
21. Mahajan Y, McArthur G (2012) Maturation of auditory event-related potentials across adolescence. Hear Res 294(1-2): 82-94.
22. Sharma A, Kraus N, McGee TJ, Nicol TG (1997) Developmental changes in P1 and N1 central auditory responses elicited by consonant-vowel syllables. Electroencephalogr Clin Neurophysiol 104(6): 540-545.
23. Eggermont JJ, Ponton CW (2003) Auditory-evoked potential studies of cortical maturation in normal hearing and implanted children: Correlations with changes in structure and speech perception. Acta Otolaryngol 123(2): 249-252.
24. Skoe E, Krizman J, Anderson S, Kraus N (2015) Stability and plasticity of auditory brainstem function across the lifespan. Cereb Cortex 25(6): 1415-1426.
25. Krizman J, et al. (2015) Continued maturation of auditory brainstem function during adolescence: A longitudinal approach. Clin Neurophysiol 2015: S1388-2457(15)00083-8.
26. Strait DL, Kraus N (2014) Biological impact of auditory expertise across the life span: Musicians as a model of auditory learning. Hear Res 308: 109-121.
27. Kraus N, Anderson S (2015) Identifying neural signatures of auditory function. Hear J 68: 38-40.
28. Kraus N, Strait DL (2015) Emergence of biological markers of musicianship with school-based music instruction. Ann N Y Acad Sci 1337: 163-169.
29. Slater J, et al. (2015) Music training improves speech-in-noise perception: Longitudinal evidence from a community-based music program. Behav Brain Res 291: 244-252.
30. Parbery-Clark A, Skoe E, Lam C, Kraus N (2009) Musician enhancement for speech-innoise. Ear Hear 30(6): 653-661.
31. Parbery-Clark A, Strait DL, Anderson S, Hittner E, Kraus N (2011) Musical experience and the aging auditory system: Implications for cognitive abilities and hearing speech in noise. PLoS One 6(5): E18082.
32. Strait DL, Parbery-Clark A, Hittner E, Kraus N (2012) Musical training during early childhood enhances the neural encoding of speech in noise. Brain Lang 123(3): 191-201.
33. Zendel BR, Alain C (2012) Musicians experience less age-related decline in central auditory processing. Psychol Aging 27(2): 410-417.
34. Swaminathan J, Mason C, Streeter T, Kidd G, Patel A (2015) Musical training, individual differences and the cocktail party problem. Scientific Reports 5: 11628.
35. Chan AS, Ho YC, Cheung MC (1998) Music training improves verbal memory. Nature 396(6707): 128.
36. Ho YC, Cheung MC, Chan AS (2003) Music training improves verbal but not visual memory: Cross-sectional and longitudinal explorations in children. Neuropsychology 17(3): 439-450.
37. Jakobson L, Lewycky S, Kilgour A, Stoesz B (2008) Memory for verbal and visual material in highly trained musicians. Music Percept 26: 21-55.
38. Tierney AT, Bergeson-Dana TR, Pisoni DB (2008) Effects of early musical experience on auditory sequence memory. Empir Musicol Rev 3(4): 178-186.
39. Kolinsky R, Cuvelier H, Goetry V, Peretz I, Morais J (2009) Music training facilitates lexical stress processing. Music Percept 26: 235-246.
40. Franois C, Chobert J, Besson M, Schön D (2013) Music training for the development of speech segmentation. Cerebral Cortex 23(9): 2038-2043.
41. Zuk J, et al. (2013) Enhanced syllable discrimination thresholds in musicians. PLoS One 8(12): E80546.
42. Overy K (2000) Dyslexia, temporal processing and music: The potential of music as an early learning aid for dyslexic children. Psychol Music 28: 218-229.
43. Degé F, Schwarzer G (2011) The effect of a music program on phonological awareness in preschoolers. Front Psychol 2: 124.
44. Herrera L, Lorenzo O, Defior S, Fernandez-Smith G, Costa-Giomi E (2011) Effects of phonological and music training on the reading readiness of native- and foreign- Spanish-speaking children. Psychol Music 39: 68-81.
45. Moritz C, Yampolsky S, Papadelis G, Thomson J, Wolf M (2013) Links between early rhythm skills, music training, and phonological awareness. Read Writ 26: 739-769.
46. Moreno S, et al. (2009) Musical training influences linguistic abilities in 8-year-old children: More evidence for brain plasticity. Cereb Cortex 19(3): 712-723.
47. Taub GE, Lazarus PJ (2012) The effects of training in timing and rhythm on reading achievement. Contemp Issues Educ Res 5: 343-350.
48. Bhide A, Power A, Goswami U (2013) A rhythmic musical intervention for poor readers: A comparison of efficacy with a letter-based intervenction. Mind Brain Educ 7: 113-123.
49. Cogo-Moreira H, Brandão de Ávila CR, Ploubidis GB, Mari JdeJ (2013) Effectiveness of music education for the improvement of reading skills and academic achievement in young poor readers: A pragmatic cluster-randomized, controlled clinical trial. PLoS One 8(3): E59984.
50. Slater J, et al. (2014) Longitudinal effects of group music instruction on literacy skills in low-income children. PLoS One 9(11): E113383.
51. Costa-Giomi E (2004) Effects of three years of piano instruction on children's academic achievement, school performance and self-esteem. Psychol Music 32: 139-152.
52. Ruggles DR, Freyman RL, Oxenham AJ (2014) Influence of musical training on understanding voiced and whispered speech in noise. PLoS One 9(1): E86980.
53. Shahin A, Bosnyak DJ, Trainor LJ, Roberts LE (2003) Enhancement of neuroplastic P2 and N1c auditory evoked potentials in musicians. J Neurosci 23(13): 5545-5552.
54. Shahin A, Roberts LE, Trainor LJ (2004) Enhancement of auditory cortical development by musical experience in children. Neuroreport 15(12): 1917-1921.
55. Musacchia G, Strait D, Kraus N (2008) Relationships between behavior, brainstem and cortical encoding of seen and heard speech in musicians and non-musicians. Hear Res 241(1-2): 34-42.
56. Franois C, Schön C (2011) Musical expertise boosts implicit learning of both musical and linguistic structures. Cereb Cortex 21(10): 2357-2365.
57. Musacchia G, Sams M, Skoe E, Kraus N (2007) Musicians have enhanced subcortical auditory and audiovisual processing of speech and music. Proc Natl Acad Sci USA 104(40): 15894-15898.
58. Parbery-Clark A, Anderson S, Hittner E, Kraus N (2012) Musical experience offsets agerelated delays in neural timing. Neurobiol Aging 33(7): 1483.e1-1483.e4.
59. Parbery-Clark A, Anderson S, Hittner E, Kraus N (2012) Musical experience strengthens the neural representation of sounds important for communication in middle-aged adults. Front Aging Neurosci 4: 30.
60. White-Schwoch T, Woodruff Carr K, Anderson S, Strait DL, Kraus N (2013) Older adults benefit from music training early in life: Biological evidence for long-term trainingdriven plasticity. J Neurosci 33(45): 17667-17674.
61. Kraus N, et al. (2014) Auditory learning through active engagement with sound: Biological impact of community music lessons in at-risk children. Front Neurosci 8: 351.
62. Parbery-Clark A, Skoe E, Kraus N (2009) Musical experience limits the degradative effects of background noise on the neural processing of sound. J Neurosci 29(45): 14100-14107.
63. Strait DL, Chan K, Ashley R, Kraus N (2012) Specialization among the specialized: Auditory brainstem function is tuned in to timbre. Cortex 48(3): 360-362.
64. Strait DL, Parbery-Clark A, O'Connell S, Kraus N (2013) Biological impact of preschool music classes on processing speech in noise. Dev Cogn Neurosci 6: 51-60.
65. Parbery-Clark A, Tierney A, Strait DL, Kraus N (2012) Musicians have fine-tuned neural distinction of speech syllables. Neuroscience 219: 111-119.
66. Strait D, O'Connell S, Parbery-Clark A, Kraus N (2014) Musicians' enhanced neural differentiation of speech sounds arises early in life: Developmental evidence from ages 3 to 30. Cereb Cortex 24(9): 2512-2521.
67. Kraus N, et al. (2014) Music enrichment programs improve the neural encoding of speech in at-risk children. J Neurosci 34(36): 11913-11918.
68. Wong PC, Skoe E, Russo NM, Dees T, Kraus N (2007) Musical experience shapes human brainstem encoding of linguistic pitch patterns. Nat Neurosci 10(4): 420-422.
69. Bidelman GM, Gandour JT, Krishnan A (2011) Cross-domain effects of music and language experience on the representation of pitch in the human auditory brainstem. J Cogn Neurosci 23(2): 425-434.
70. Skoe E, Kraus N (2013) Musical training heightens auditory brainstem function during sensitive periods in development. Front Psychol 4: 622.
71. Tierney A, Krizman J, Skoe E, Johnston K, Kraus N (2013) High school music classes enhance the neural processing of speech. Front Psychol 4: 855.
72. Hakuta K, Bialystok E, Wiley E (2003) Critical evidence: A test of the critical-period hypothesis for second-language acquisition. Psychol Sci 14(1): 31-38.
73. Hornickel J, Kraus N (2013) Unstable representation of sound: A biological marker of dyslexia. J Neurosci 33(8): 3500-3504.
74. Whitford TJ, et al. (2007) Brain maturation in adolescence: Concurrent changes in neuroanatomy and neurophysiology. Hum Brain Mapp 28(3): 228-237.
75. Hornickel J, Zecker SG, Bradlow AR, Kraus N (2012) Assistive listening devices drive neuroplasticity in children with dyslexia. Proc Natl Acad Sci USA 109(41): 16731-16736.
76. Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23(6): 251-258.
77. Seppänen M, Hämäläinen J, Pesonen AK, Tervaniemi M (2012) Music training enhances rapid neural plasticity of n1 and p2 source activation for unattended sounds. Front Hum Neurosci 6: 43.
78. Slevc LR, Miyake A (2006) Individual differences in second-language proficiency: Does musical ability matter? Psychol Sci 17(8): 675-681.
79. Penhune VB (2011) Sensitive periods in human development: Evidence from musical training. Cortex 47(9): 1126-1137.
80. Recanzone GH, Schreiner CE, Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 13(1): 87-103.
81. Blake DT, Heiser MA, Caywood M, MerzenichMM (2006) Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward. Neuron 52(2): 371-381.
82. Xiong Y, Zhang Y, Yan J (2009) The neurobiology of sound-specific auditory plasticity: A core neural circuit. Neurosci Biobehav Rev 33(8): 1178-1184.
83. Patel AD (2011) Why would music training benefit the neural encoding of speech? The OPERA hypothesis. Front Psychol 2: 142.
84. Salimpoor VN, et al. (2013) Interactions between the nucleus accumbens and auditory cortices predict music reward value. Science 340(6129): 216-219.
85. Thomson J, Fryer B, Maltby J, Goswami U (2006) Auditory and motor rhythm awareness in adults with dyslexia. J Res Read 29: 334-348.
86. Thomson JM, Goswami U (2008) Rhythmic processing in children with developmental dyslexia: Auditory and motor rhythms link to reading and spelling. J Physiol Paris 102(1-3): 120-129.
87. Corriveau KH, Goswami U (2009) Rhythmic motor entrainment in children with speech and language impairments: Tapping to the beat. Cortex 45(1): 119-130.
88. Tierney A, Kraus N (2014) Auditory-motor entrainment and phonological skills: Precise auditory timing hypothesis (PATH). Front Hum Neurosci 8: 949.
89. Norton ES, Wolf M (2012) Rapid automatized naming (RAN) and reading fluency: Implications for understanding and treatment of reading disabilities. Annu Rev Psychol 63: 427-452.
90. Krizman J, Skoe E, Kraus N (2012) Sex differences in auditory subcortical function. Clin Neurophysiol 123(3): 590-597.
91. Skoe E, Krizman J, Kraus N (2013) The impoverished brain: Disparities in maternal education affect the neural response to sound. J Neurosci 33(44): 17221-17231.
92. Rabkin N, Hedberg EC (2011) Arts Education in America: What the Declines Mean for Arts Participation (National Endowment for the Arts, Washington, DC), Research Report 52 (Based on the 2008 Survey of Public Participation in the Arts).
93. Green CS, Bavelier D (2012) Learning, attentional control, and action video games. Curr Biol 22(6): R197-R206.
94. Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence (Psychological Corporation, San Antonio, TX).
95. Liu LF, Palmer AR, Wallace MN (2006) Phase-locked responses to pure tones in the inferior colliculus. J Neurophysiol 95(3): 1926-1935.
96. Chandrasekaran B, Kraus N (2010) The scalp-recorded brainstem response to speech: Neural origins and plasticity. Psychophysiology 47(2): 236-246.
97. Delorme A, Makeig S (2004) EEGLAB: An open source toolbox for analysis of singletrial EEG dynamics including independent component analysis. J Neurosci Methods 134(1): 9-21.
98. Lopez-Calderon J, Luck SJ (2014) ERPLAB: An open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci 8: 213.
99. Wagner R, Torgesen J, Rashotte C (1999) CTOPP: Comprehensive Test of Phonological Processing (Pro-ed, Austin, TX).