Musicians' enhanced neural differentiation of speech sounds arises early in life: Developmental evidence from ages 3 to 30

Cerebral Cortex

Volumn 24, Issue 9, 2014, Pages 2512-2521

  Strait, Dana L ^a   O'Connell, Samantha ^a   Parbery Clark, Alexandra ^a   Kraus, Nina ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Attention; Auditory; Brain; Language; Musical training

Indexed keywords

ADOLESCENT; ADULT; AGE DISTRIBUTION; ARTICLE; ATTENTION; AUDITORY MEMORY; CHILD; COGNITION; CONSONANT; EVOKED BRAIN STEM AUDITORY RESPONSE; HEARING; HUMAN; HUMAN EXPERIMENT; LEARNING; MUSIC; MUSICIAN; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NORMAL HUMAN; PRESCHOOL CHILD; PRIORITY JOURNAL; SCHOOL CHILD; SPEECH DEVELOPMENT; SPEECH PERCEPTION; STIMULUS RESPONSE; TRAINING; VISION; WORKING MEMORY; BRAIN STEM; GROWTH, DEVELOPMENT AND AGING; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; SHORT TERM MEMORY; SOUND DETECTION; SPEECH; YOUNG ADULT;

ADOLESCENT; ADULT; ATTENTION; BRAIN STEM; CHILD; CHILD, PRESCHOOL; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; HUMANS; MEMORY, SHORT-TERM; MUSIC; NEUROPSYCHOLOGICAL TESTS; PRACTICE (PSYCHOLOGY); SOUND SPECTROGRAPHY; SPEECH ACOUSTICS; SPEECH PERCEPTION; YOUNG ADULT;

EID: 84906973219     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht103     Document Type: Article

References (85)

1. Aiken SJ, Picton TW. 2008. Envelope and spectral frequency-following responses to vowel sounds. Hear Res. 245:35-47.
2. Akhoun I, Gallego S, Moulin A, Menard M, Veuillet E, Berger-Vachon C, Collet L, Thai-Van H. 2008. The temporal relationship between speech auditory brainstem responses and the acoustic pattern of the phoneme /ba/ in normal-hearing adults. Clin Neurophysiol. 119:922-933.
3. Anvari SH, Trainor LJ, Woodside J, Levy BA. 2002. Relations among musical skills, phonological processing, and early reading ability in preschool children. J Exp Child Psychol. 83:111-130. (Pubitemid 39659808)
4. Bajo VM, Nodal FR, Moore DR, King AJ. 2010. The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nat Neurosci. 13:253-260.
5. Banai K, Hornickel JM, Skoe E, Nicol T, Zecker S, Kraus N. 2009. Reading and subcortical auditory function. Cereb Cortex. 19:2699-2707.
6. Barry JG, Ferguson MA, Moore DR. 2010. Making sense of listening: the IMAP test battery. J Vis Exp. 44.
7. Bauerle P, von der Behrens W, Kossl M, Gaese BH. 2011. Stimulus-specific adaptation in the gerbil primary auditory thalamus is the result of a fast frequency-specific habituation and is regulated by the corticofugal system. J Neurosci. 31:9708-9722.
8. Bidelman GM, Gandour JT, Krishnan A. 2009. Cross-domain effects of music and language experience on the representation of pitch in the human auditory brainstem. J Cogn Neurosci. 23:425-434.
9. Bidelman GM, Krishnan A. 2010. Effects of reverberation on brain-stem representation of speech in musicians and non-musicians. Brain Res. 1355:112-125.
10. Billiet CR, Bellis TJ. 2011. The relationship between brainstem temporal processing and performance on tests of central auditory function in children with reading disorders. J Speech Lang Hear Res. 54:228-242.
11. Bradley L, Bryant PE. 1983. Categorising sounds and learning to read: a causal connection. Nature. 310:419-421. (Pubitemid 13160554)
12. Brown L, Sherbenou RJ, Johnsen SK. 1997. Test of Nonverbal Intelligence (TONI-3). Austin (TX): Pro-Ed, Inc.
13. Chandrasekaran B, Hornickel J, Skoe E, Nicol T, Kraus N. 2009. Context-dependent encoding in the human auditory brainstem relates to hearing speech in noise: implications for developmental dyslexia. Neuron. 64:311-319.
14. Chobert J, Francois C, Habib M, Besson M. 2012. Deficit in the preattentive processing of syllabic duration and VOT in children with dyslexia. Neuropsychologia. 50:2044-2055.
15. Chobert J, Francois C, Velay JL, Besson M. 2012. Twelve months of active musical training in 8- to 10-year-old children enhances the preattentive processing of syllabic duration and voice onset time. Cereb Cortex. doi: 10.1093/cercor/bhs377.
16. Chobert J, Marie C, Francois C, Schon D, Besson M. 2011. Enhanced passive and active processing of syllables in musician children. J Cogn Neurosci. 23:3874-3887.
17. Crottaz-Herbette S, Menon V. 2006. Where and when the anterior cingulate cortex modulates attentional response: combined fMRI and ERP evidence. J Cogn Neurosci. 18:766-780.
18. Davis HP, Keller F. 2002. Colorado assessment tests (CATS), version 1.2. Colorado Springs (CO): Colorado Assessment Tests.
19. Dege F, Schwarzer G. 2011. The effect of a music program on phonological awareness in preschoolers. Front Psychol. 2:124.
20. Dunn LM, Dunn LM. 1997. Peabody picture vocabulary test. 3rd ed. San Antonio (TX): Pearson Education, Inc.
21. Engineer ND, Percaccio CR, Pandya PK, Moucha R, Rathbun DL, Kilgard MP. 2004. Environmental enrichment improves response strength, threshold, selectivity, and latency of auditory cortex neurons. J Neurophysiol. 92:73-82. (Pubitemid 38802234)
22. Francois C, Chobert J, Besson M, Schon D. 2012. Music training for the development of speech segmentation. Cereb Cortex. (Epub ahead of print). doi: 10.1093/cercor/bhs180.
23. Fritz JB, David SV, Radtke-Schuller S, Yin P, Shamma SA. 2010. Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex. Nat Neurosci. 13:1011-1019.
24. Fritz JB, Elhilali M, David SV, Shamma SA. 2007. Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1? Hear Res. 229:186-203. (Pubitemid 46924825)
25. Fritz JB, Elhilali M, Shamma SA. 2007. Adaptive changes in cortical receptive fields induced by attention to complex sounds. J Neurophysiol. 98:2337-2346. (Pubitemid 47584416)
26. Gleeson JG, Walsh CA. 2000. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci. 23:352-359. (Pubitemid 30628811)
27. Harrison RV, Gordon KA, Mount RJ. 2005. Is there a critical period for cochlear implantation in congenitally deaf children? Analyses of hearing and speech perception performance after implantation. Dev Psychobiol. 46:252-261. (Pubitemid 40592654)
28. Hazan V, Barrett S. 2000. The development of phonemic categorization in children aged 6-12. J Phonetics. 28:377-396.
29. Hornickel J, Chandrasekaran B, Zecker S, Kraus N. 2011. Auditory brainstem measures predict reading and speech-in-noise perception in school-aged children. Behav Brain Res. 216:597-605.
30. Hornickel J, Lin D, Kraus N. 2013. Speech-evoked auditory brainstem responses reflect familial and cognitive influences. Dev Sci. 16:101-110.
31. Hornickel J, Skoe E, Nicol T, Zecker S, Kraus N. 2009. Subcortical differentiation of voiced stop consonants: relationships to reading and speech in noise perception. Proc Natl Acad Sci USA. 106:13022-13027.
32. Houston DM, Miyamoto RT. 2010. Effects of early auditory experience on word learning and speech perception in deaf children with cochlear implants: implications for sensitive periods of language development. Otol Neurotol. 31:1248-1253.
33. Ji W, Suga N. 2009. Tone-specific and nonspecific plasticity of inferior colliculus elicited by pseudo-conditioning: role of acetylcholine and auditory and somatosensory cortices. J Neurophysiol. 102:941-952.
34. Johnson KL, Nicol T, Zecker SG, Kraus N. 2008. Developmental plasticity in the human auditory brainstem. J Neurosci. 28:4000-4007.
35. Klatt D. 1980. Software for a cascade/parallel formant synthesizer. J Acoust Soc Amer. 67:13-33.
36. Kral A, Eggermont JJ. 2007. What's to lose and what's to learn: development under auditory deprivation, cochlear implants and limits of cortical plasticity. Brain Res Rev. 56:259-269. (Pubitemid 350100872)
37. Kraus N, Chandrasekaran B. 2010. Music training for the development of auditory skills. Nat Rev Neurosci. 11:599-605.
38. Kraus N, McGee T, Carrell TD, Sharma A. 1995. Neurophysiologic bases of speech discrimination. Ear Hear. 16:19-37.
39. Kraus N, McGee TJ, Carrell TD, Zecker SG, Nicol TG, Koch DB. 1996. Auditory neurophysiologic responses and discrimination deficits in children with learning problems. Science. 273:971-973. (Pubitemid 26275177)
40. Kraus N, Strait DL, Parbery-Clark A. 2012. Cognitive factors shape brain networks for auditory skills: spotlight on auditory working memory. Ann N Y Acad Sci. 1252:100-107.
41. Krizman J, Marian V, Shook A, Skoe E, Kraus N. 2012. Subcortical encoding of sound is enhanced in bilinguals and relates to executive function advantages. Proc Natl Acad Sci USA. 109:7877-7881.
42. Luo F, Wang Q, Kashani A, Yan J. 2008. Corticofugal modulation of initial sound processing in the brain. J Neurosci. 28:11615-11621.
43. Macedo CE, Cuadra G, Molina V, Brandao ML. 2005. Aversive stimulation of the inferior colliculus changes dopamine and serotonin extracellular levels in the frontal cortex: modulation by the basolateral nucleus of amygdala. Synapse. 55:58-66. (Pubitemid 39565228)
44. Marsh RA, Fuzessery ZM, Grose CD, Wenstrup JJ. 2002. Projection to the inferior colliculus from the basal nucleus of the amygdala. J Neurosci. 22:10449-10460. (Pubitemid 35416881)
45. Milovanov R, Huotilainen M, Esquef PA, Alku P, Valimaki V, Tervaniemi M. 2009. The role of musical aptitude and language skills in preattentive duration processing in school-aged children. Neurosci Lett. 460:161-165.
46. Milovanov R, Huotilainen M, Valimaki V, Esquef PA, Tervaniemi M. 2008. Musical aptitude and second language pronunciation skills in school-aged children: neural and behavioral evidence. Brain Res. 1194:81-89.
47. Milovanov R, Pietila P, Tervaniemi M, Esquef PA. 2010. Foreign language pronunciation skills and musical aptitude: a study of Finnish adults with higher education. Learn Indiv Diff. 20:56-60.
48. Moore JK, Guan YL. 2001. Cytoarchitectural and axonal maturation in human auditory cortex. J Assoc Res Otolaryngol. 2:297-311. (Pubitemid 34074312)
49. Moore JK, Linthicum FH Jr. 2007. The human auditory system: a timeline of development. Int J Audiol. 46:460-478. (Pubitemid 350194919)
50. Moore JK, Perazzo LM, Braun A. 1995. Time course of axonal myelination in the human brainstem auditory pathway. Hear Res. 87:21-31.
51. Moreno S, Marques C, Santos A, Santos M, Castro SL, Besson M. 2009. Musical training influences linguistic abilities in 8-year-old children: more evidence for brain plasticity. Cereb Cortex. 19:712-723.
52. Morris JS, Friston KJ, Dolan RJ. 1998. Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proc Biol Sci. 265:649-657. (Pubitemid 28200758)
53. 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. 104:15894-15898. (Pubitemid 350035395)
54. Nittrouer S, Miller ME. 1997. Predicting developmental shifts in perceptual weighting schemes. J Acoust Soc Am. 101:2253-2266. (Pubitemid 27163989)
55. Norena AJ, Gourevitch B, Aizawa N, Eggermont JJ. 2006. Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex. Nat Neurosci. 9:932-939. (Pubitemid 43980508)
56. Overy K, Nicolson RI, Fawcett AJ, Clarke EF. 2003. Dyslexia and music: measuring musical timing skills. Dyslexia. 9:18-36. (Pubitemid 40309217)
57. Pandya DN, Van Hoesen GW, Mesulam MM. 1981. Efferent connections of the cingulate gyrus in the rhesus monkey. Exp Brain Res. 42:319-330. (Pubitemid 11112361)
58. Parbery-Clark A, Anderson S, Hittner E, Kraus N. 2012a. Musical experience offsets age-related delays in neural timing. Neurobiol Aging. 33:1483.e1.-1483.e4.
59. Parbery-Clark A, Anderson S, Hittner E, Kraus N. 2012b. Musical experience strengthens the neural representation of sounds important for communication in middle-aged adults. Front Aging Neurosci. 4:1-12.
60. 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. 29:14100-14107.
61. Parbery-Clark A, Strait DL, Kraus N. 2011. Context-dependent encoding in the auditory brainstem subserves enhanced speech-in-noise perception in musicians. Neuropsychologia. 49:3338-3345.
62. Parbery-Clark A, Tierney A, Strait DL, Kraus N. 2012. Musicians have fine-tuned neural distinction of speech syllables. Neuroscience. 219:111-119.
63. Patel AD. 2011. Why would musical training benefit the neural encoding of speech? The OPERA hypothesis. Front Psychol. 2:142.
64. Rocha-Muniz CN, Befi-Lopes DM, Schochat E. 2012. Investigation of auditory processing disorder and language impairment using the speech-evoked auditory brainstem response. Hear Res. 294:143-152.
65. Shook A, Marian V, Bartolotti J, Schroeder S. 2013. Musical experience influences novel language learning. Am J Psychol. 126:95-104.
66. Siok WT, Fletcher P. 2001. The role of phonological awareness and visual-orthographic skills in Chinese reading acquisition. Dev Psychol. 37:886-899.
67. Skoe E, Kraus N. 2010. Auditory brain stem response to complex sounds: a tutorial. Ear Hear. 31(3):302-324.
68. Skoe E, Kraus N. 2012. A little goes a long way: how the adult brain is shaped by musical training in childhood. J Neurosci. 32:11507-11510.
69. Skoe E, Nicol T, Kraus N. 2011. Cross-phaseogram: objective neural index of speech sound differentiation. J Neurosci Methods. 196:308-317.
70. Slevc LR, Miyake A. 2006. Individual differences in second-language proficiency: does musical ability matter? Psychol Sci. 17:675-681. (Pubitemid 44179877)
71. Stevens C, Lauinger B, Neville H. 2009. Differences in the neural mechanisms of selective attention in children from different socioeconomic backgrounds: an event-related brain potential study. Dev Sci. 12:634-646.
72. Strait DL, Hornickel J, Kraus N. 2011. Subcortical processing of speech regularities underlies reading and music aptitude in children. Behav Brain Funct. 7:44.
73. Strait DL, Kraus N. 2011. Playing music for a smarter ear: cognitive, perceptual and neurobiological evidence. Music Percept. 29:133-147.
74. Strait DL, Kraus N, Parbery-Clark A, Ashley R. 2010. Musical experience shapes top-down auditory mechanisms: evidence from masking and auditory attention performance. Hear Res. 261:22-29.
75. Strait DL, Kraus N, Skoe E, Ashley R. 2009. Musical experience and neural efficiency: effects of training on subcortical processing of vocal expressions of emotion. Eur J Neurosci. 29:661-668.
76. 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. 123:191-201.
77. Taniguchi I. 1981. Plastic changes in the inferior colliculus following cochlear destruction. In: Syka J, Aitkin L, editors. Neuronal mechanisms of hearing. New York (NY): Plenum Press. p. 377-380.
78. Wechsler D. 1999. Wechsler abbreviated scale of intelligence (WASI). San Antonio (TX): Harcourt Assessment.
79. Weinberger NM. 2004. Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci. 5:279-290. (Pubitemid 38478655)
80. Wong PC, Skoe E, Russo NM, Dees T, Kraus N. 2007. Musical experience shapes human brainstem encoding of linguistic pitch patterns. Nat Neurosci. 10:420-422. (Pubitemid 46494592)
81. Woodcock RW, McGre KS, Mather N. 2001. Woodcock-Johnson psycho-educational battery. 3rd edn. Itasca (IL): Riverside.
82. Yan J, Zhang Y. 2005. Sound-guided shaping of the receptive field in the mouse auditory cortex by basal forebrain activation. Eur J Neurosci. 21:563-576. (Pubitemid 40204260)
83. Yan J, Zhang Y, Ehret G. 2005. Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. J Neurophysiol. 93:71-83. (Pubitemid 40626823)
84. Zhang Y, Hakes JJ, Bonfield SP, Yan J. 2005. Corticofugal feedback for auditory midbrain plasticity elicited by tones and electrical stimulation of basal forebrain in mice. Eur J Neurosci. 22:871-879. (Pubitemid 41243328)
85. Zwolan TA, Ashbaugh CM, Alarfaj A, Kileny PR, Arts HA, El-Kashlan HK, Telian SA. 2004. Pediatric cochlear implant patient performance as a function of age at implantation. Otol Neurotol. 25:112-120. (Pubitemid 39079837)