Brain Structure and Function

, Volume 223, Issue 4, pp 2013–2024 | Cite as

The lateralized arcuate fasciculus in developmental pitch disorders among mandarin amusics: left for speech and right for music

  • Xizhuo Chen
  • Yanxin Zhao
  • Suyu Zhong
  • Zaixu Cui
  • Jiaqi Li
  • Gaolang Gong
  • Qi Dong
  • Yun Nan
Original Article

Abstract

The arcuate fasciculus (AF) is a neural fiber tract that is critical to speech and music development. Although the predominant role of the left AF in speech development is relatively clear, how the AF engages in music development is not understood. Congenital amusia is a special neurodevelopmental condition, which not only affects musical pitch but also speech tone processing. Using diffusion tensor tractography, we aimed at understanding the role of AF in music and speech processing by examining the neural connectivity characteristics of the bilateral AF among thirty Mandarin amusics. Compared to age- and intelligence quotient (IQ)-matched controls, amusics demonstrated increased connectivity as reflected by the increased fractional anisotropy in the right posterior AF but decreased connectivity as reflected by the decreased volume in the right anterior AF. Moreover, greater fractional anisotropy in the left direct AF was correlated with worse performance in speech tone perception among amusics. This study is the first to examine the neural connectivity of AF in the neurodevelopmental condition of amusia as a result of disrupted music pitch and speech tone processing. We found abnormal white matter structural connectivity in the right AF for the amusic individuals. Moreover, we demonstrated that the white matter microstructural properties of the left direct AF is modulated by lexical tone deficits among the amusic individuals. These data support the notion of distinctive pitch processing systems between music and speech.

Keywords

Diffusion tensor imaging Congenital amusia Pitch processing Connectivity Lexical tone processing 

Notes

Acknowledgements

This work was supported by the 973 Program [2014CB846103], the National Natural Science Foundation of China [31471066, 31221003 and 31521063], the 111 project [B07008], Beijing Municipal Science & Technology Commission [Z151100003915122], the Interdiscipline Research Funds of Beijing Normal University, and the Fundamental Research Funds for the Central Universities. We owe our thanks to members of the music group at the State Key Laboratory of Cognitive Neuroscience and Learning for their input. We thank the participants for their support. We thank the reviewers for their valuable and insightful comments.

References

  1. Albouy P, Mattout J, Bouet R, Maby E, Sanchez G, Aguera PE, Daligault S, Delpuech C, Bertrand O, Caclin A, Tillmann B (2013) Impaired pitch perception and memory in congenital amusia: the deficit starts in the auditory cortex. Brain 136(Pt 5):1639–1661.  https://doi.org/10.1093/brain/awt082 CrossRefPubMedGoogle Scholar
  2. Ashtari M, Cervellione KL, Hasan KM, Wu J, McIlree C, Kester H, Ardekani BA, Roofeh D, Szeszko PR, Kumra S (2007) White matter development during late adolescence in healthy males: a cross-sectional diffusion tensor imaging study. Neuroimage 35(2):501–510.  https://doi.org/10.1016/j.neuroimage.2006.10.047 CrossRefPubMedGoogle Scholar
  3. Bizzi A, Nava S, Ferre F, Castelli G, Aquino D, Ciaraffa F, Broggi G, DiMeco F, Piacentini S (2012) Aphasia induced by gliomas growing in the ventrolateral frontal region: assessment with diffusion MR tractography, functional MR imaging and neuropsychology. Cortex 48(2):255–272.  https://doi.org/10.1016/j.cortex.2011.11.015 CrossRefPubMedGoogle Scholar
  4. Brancucci A, Franciotti R, D’Anselmo A, Della Penna S, Tommasi L (2011) The sound of consciousness: neural underpinnings of auditory perception. J Neurosci 31(46):16611–16618.  https://doi.org/10.1523/JNEUROSCI.3949-11.2011 CrossRefPubMedGoogle Scholar
  5. Casserly ED, Pisoni DB (2010) Speech perception and production. Wiley interdisciplinary reviews cognitive science 1 (5):pp 629–647.  https://doi.org/10.1002/wcs.63
  6. Catani M, Bambini V (2014) A model for social communication and language evolution and development (SCALED). Curr Opin Neurobiol 28:165–171.  https://doi.org/10.1016/j.conb.2014.07.018 CrossRefPubMedGoogle Scholar
  7. Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44(8):1105–1132.  https://doi.org/10.1016/j.cortex.2008.05.004 CrossRefPubMedGoogle Scholar
  8. Catani M, Jones DK, ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57(1):8–16.  https://doi.org/10.1002/ana.20319 CrossRefPubMedGoogle Scholar
  9. Catani M, Allin MP, Husain M, Pugliese L, Mesulam MM, Murray RM, Jones DK (2007) Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci USA 104(43):17163–17168.  https://doi.org/10.1073/pnas.0702116104 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chen JL, Kumar S, Williamson VJ, Scholz J, Griffiths TD, Stewart L (2015) Detection of the arcuate fasciculus in congenital amusia depends on the tractography algorithm. Front Psychol 6:9.  https://doi.org/10.3389/fpsyg.2015.00009 PubMedPubMedCentralGoogle Scholar
  11. Christodoulou JA, Murtagh J, Cyr A, Perrachione TK, Chang P, Halverson K, Hook P, Yendiki A, Ghosh S, Gabrieli JD (2016) Relation of White-Matter Microstructure to Reading Ability and Disability in Beginning Readers. Neuropsychology.  https://doi.org/10.1037/neu0000243 PubMedGoogle Scholar
  12. Cui Z, Zhong S, Xu P, He Y, Gong G (2013) PANDA: a pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci 7:42.  https://doi.org/10.3389/fnhum.2013.00042 PubMedPubMedCentralGoogle Scholar
  13. Dick AS, Tremblay P (2012) Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain 135 (Pt 12):3529–3550.  https://doi.org/10.1093/brain/aws222
  14. Forkel SJ, Thiebaut de Schotten M, Dell’Acqua F, Kalra L, Murphy DG, Williams SC, Catani M (2014) Anatomical predictors of aphasia recovery: a tractography study of bilateral perisylvian language networks. Brain 137(Pt 7):2027–2039.  https://doi.org/10.1093/brain/awu113 CrossRefPubMedGoogle Scholar
  15. Foxton JM, Dean JL, Gee R, Peretz I, Griffiths TD (2004) Characterization of deficits in pitch perception underlying ‘tone deafness’. Brain 127(Pt 4):801–810.  https://doi.org/10.1093/brain/awh105 CrossRefPubMedGoogle Scholar
  16. Fridriksson J, Guo D, Fillmore P, Holland A, Rorden C (2013) Damage to the anterior arcuate fasciculus predicts non-fluent speech production in aphasia. Brain 136(Pt 11):3451–3460.  https://doi.org/10.1093/brain/awt267 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Friederici AD (2012) Language development and the ontogeny of the dorsal pathway. Front Evolut Neurosci 4:3.  https://doi.org/10.3389/fnevo.2012.00003 Google Scholar
  18. Gandour J, Wong D, Hsieh L, Weinzapfel B, Van Lancker D, Hutchins GD (2000) A crosslinguistic PET study of tone perception. J Cogn Neurosci 12(1):207–222CrossRefPubMedGoogle Scholar
  19. Glasser MF, Rilling JK (2008) DTI tractography of the human brain’s language pathways. Cereb Cortex 18(11):2471–2482.  https://doi.org/10.1093/cercor/bhn011 CrossRefPubMedGoogle Scholar
  20. Gong Y, Cai T (1993) Manual of Chinese revised Wechsler intelligence scale for children. Hunan Atlas Publishing House, ChangshaGoogle Scholar
  21. Halwani GF, Loui P, Ruber T, Schlaug G (2011) Effects of practice and experience on the arcuate fasciculus: comparing singers, instrumentalists, and non-musicians. Front Psychol 2:156.  https://doi.org/10.3389/fpsyg.2011.00156 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8(5):393–402.  https://doi.org/10.1038/nrn2113 CrossRefPubMedGoogle Scholar
  23. Huang WT, Liu C, Dong Q, Nan Y (2015a) Categorical perception of lexical tones in mandarin-speaking congenital amusics. Front Psychol 6:829.  https://doi.org/10.3389/fpsyg.2015.00829 PubMedPubMedCentralGoogle Scholar
  24. Huang WT, Nan Y, Dong Q, Liu C (2015b) Just-noticeable difference of tone pitch contour change for Mandarin congenital amusics. J Acoust Soc Am 138(1):EL99–E104.  https://doi.org/10.1121/1.4923268 CrossRefPubMedGoogle Scholar
  25. Hyde KL, Peretz I (2004) Brains that are out of tune but in time. Psychol Sci 15(5):356–360.  https://doi.org/10.1111/j.0956-7976.2004.00683.x CrossRefPubMedGoogle Scholar
  26. Hyde KL, Zatorre RJ, Griffiths TD, Lerch JP, Peretz I (2006) Morphometry of the amusic brain: a two-site study. Brain 129(Pt 10):2562–2570.  https://doi.org/10.1093/brain/awl204 CrossRefPubMedGoogle Scholar
  27. Hyde KL, Zatorre RJ, Peretz I (2011) Functional MRI evidence of an abnormal neural network for pitch processing in congenital amusia. Cereb Cortex 21(2):292–299.  https://doi.org/10.1093/cercor/bhq094 CrossRefPubMedGoogle Scholar
  28. Jones DK (2003) Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI. Magn Reson Med 49(1):7–12.  https://doi.org/10.1002/mrm.10331 CrossRefPubMedGoogle Scholar
  29. Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254.  https://doi.org/10.1016/j.neuroimage.2012.06.081 CrossRefPubMedGoogle Scholar
  30. Klein D, Zatorre RJ, Milner B, Zhao V (2001) A cross-linguistic PET study of tone perception in Mandarin Chinese and English speakers. Neuroimage 13(4):646–653.  https://doi.org/10.1006/nimg.2000.0738 CrossRefPubMedGoogle Scholar
  31. Langer N, Peysakhovich B, Zuk J, Drottar M, Sliva DD, Smith S, Becker BL, Grant PE, Gaab N (2015) White matter alterations in infants at risk for developmental dyslexia. Cereb Cortex.  https://doi.org/10.1093/cercor/bhv281 PubMedGoogle Scholar
  32. Liberman AM, Harris KS, Hoffman HS, Griffith BC (1957) The discrimination of speech sounds within and across phoneme boundaries. J Exp Psychol 54(5):358–368CrossRefPubMedGoogle Scholar
  33. Liu F, Jiang C, Thompson WF, Xu Y, Yang Y, Stewart L (2012) The mechanism of speech processing in congenital amusia: evidence from Mandarin speakers. PLoS One 7(2):e30374.  https://doi.org/10.1371/journal.pone.0030374 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Liu F, Chan AH, Ciocca V, Roquet C, Peretz I, Wong PC (2016) Pitch perception and production in congenital amusia: evidence from Cantonese speakers. J Acoust Soc Am 140(1):563.  https://doi.org/10.1121/1.4955182 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lopez-Barroso D, Catani M, Ripolles P, Dell’Acqua F, Rodriguez-Fornells A, de Diego-Balaguer R (2013) Word learning is mediated by the left arcuate fasciculus. Proc Natl Acad Sci USA 110(32):13168–13173.  https://doi.org/10.1073/pnas.1301696110 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Loui P, Alsop D, Schlaug G (2009) Tone deafness: a new disconnection syndrome? J Neurosci 29(33):10215–10220.  https://doi.org/10.1523/JNEUROSCI.1701-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Loui P, Demorest SM, Pfordresher PQ, Iyer J (2015) Neurological and developmental approaches to poor pitch perception and production. Ann N Y Acad Sci 1337:263–271.  https://doi.org/10.1111/nyas.12623 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Mignault Goulet G, Moreau P, Robitaille N, Peretz I (2012) Congenital amusia persists in the developing brain after daily music listening. PLoS One 7(5):e36860.  https://doi.org/10.1371/journal.pone.0036860 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nan Y, Friederici AD (2013) Differential roles of right temporal cortex and Broca’s area in pitch processing: evidence from music and Mandarin. Hum Brain Mapp 34(9):2045–2054.  https://doi.org/10.1002/hbm.22046 CrossRefPubMedGoogle Scholar
  40. Nan Y, Sun Y, Peretz I (2010) Congenital amusia in speakers of a tone language: association with lexical tone agnosia. Brain 133(9):2635–2642.  https://doi.org/10.1093/brain/awq178 CrossRefPubMedGoogle Scholar
  41. Nan Y, Huang WT, Wang WJ, Liu C, Dong Q (2016) Subgroup differences in the lexical tone mismatch negativity (MMN) among Mandarin speakers with congenital amusia. Biol Psychol 113:59–67.  https://doi.org/10.1016/j.biopsycho.2015.11.010 CrossRefPubMedGoogle Scholar
  42. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113CrossRefPubMedGoogle Scholar
  43. Omigie D, Pearce MT, Williamson VJ, Stewart L (2013) Electrophysiological correlates of melodic processing in congenital amusia. Neuropsychologia 51(9):1749–1762.  https://doi.org/10.1016/j.neuropsychologia.2013.05.010 CrossRefPubMedGoogle Scholar
  44. Pardo JS (2006) On phonetic convergence during conversational interaction. J Acoust Soc Am 119(4):2382–2393CrossRefPubMedGoogle Scholar
  45. Peretz I, Vuvan DT (2017) Prevalence of congenital amusia. Eur J Hum Genetics: EJHG 25(5):625–630.  https://doi.org/10.1038/ejhg.2017.15 CrossRefGoogle Scholar
  46. Peretz I, Ayotte J, Zatorre RJ, Mehler J, Ahad P, Penhune VB, Jutras B (2002) Congenital amusia: a disorder of fine-grained pitch discrimination. Neuron 33(2):185–191 pii]CrossRefPubMedGoogle Scholar
  47. Peretz I, Champod AS, Hyde K (2003) Varieties of musical disorders. The montreal battery of evaluation of amusia. Ann N Y Acad Sci 999:58–75CrossRefPubMedGoogle Scholar
  48. Peretz I, Brattico E, Jarvenpaa M, Tervaniemi M (2009) The amusic brain: in tune, out of key, and unaware. Brain 132(Pt 5):1277–1286.  https://doi.org/10.1093/brain/awp055 CrossRefPubMedGoogle Scholar
  49. Rauschecker JP (2012) Ventral and dorsal streams in the evolution of speech and language. Frontiers in evolutionary neuroscience 4:7.  https://doi.org/10.3389/fnevo.2012.00007 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Schaechter JD, Fricker ZP, Perdue KL, Helmer KG, Vangel MG, Greve DN, Makris N (2009) Microstructural status of ipsilesional and contralesional corticospinal tract correlates with motor skill in chronic stroke patients. Hum Brain Mapp 30(11):3461–3474.  https://doi.org/10.1002/hbm.20770 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Schlaug G, Marchina S, Norton A (2009) Evidence for plasticity in white-matter tracts of patients with chronic Broca’s aphasia undergoing intense intonation-based speech therapy. Ann N Y Acad Sci 1169:385–394.  https://doi.org/10.1111/j.1749-6632.2009.04587.x CrossRefPubMedPubMedCentralGoogle Scholar
  52. Song S-K, Sun S-W, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 17(3):1429–1436.  https://doi.org/10.1006/nimg.2002.1267 CrossRefPubMedGoogle Scholar
  53. Tak HJ, Kim JH, Son SM (2016) Developmental process of the arcuate fasciculus from infancy to adolescence: a diffusion tensor imaging study. Neural Regeneration Res 11(6):937–943.  https://doi.org/10.4103/1673-5374.184492 Google Scholar
  54. Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DG, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54(1):49–59.  https://doi.org/10.1016/j.neuroimage.2010.07.055 CrossRefPubMedGoogle Scholar
  55. Thiebaut de Schotten M, Cohen L, Amemiya E, Braga LW, Dehaene S (2014) Learning to read improves the structure of the arcuate fasciculus. Cereb Cortex 24(4):989–995.  https://doi.org/10.1093/cercor/bhs383 CrossRefPubMedGoogle Scholar
  56. Tillmann B, Burnham D, Nguyen S, Grimault N, Gosselin N, Peretz I (2011) Congenital Amusia (or Tone-Deafness) Interferes with Pitch Processing in Tone Languages. Front Psychol 2:120.  https://doi.org/10.3389/fpsyg.2011.00120 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Tillmann B, Gosselin N, Bigand E, Peretz I (2012) Priming paradigm reveals harmonic structure processing in congenital amusia. Cortex 48(8):1073–1078.  https://doi.org/10.1016/j.cortex.2012.01.001 CrossRefPubMedGoogle Scholar
  58. Tremblay P, Dick AS (2016) Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain Lang 162:60–71.  https://doi.org/10.1016/j.bandl.2016.08.004 CrossRefPubMedGoogle Scholar
  59. Van Beek L, Ghesquiere P, Lagae L, De Smedt B (2014) Left fronto-parietal white matter correlates with individual differences in children’s ability to solve additions and multiplications: a tractography study. Neuroimage 90:117–127.  https://doi.org/10.1016/j.neuroimage.2013.12.030 CrossRefPubMedGoogle Scholar
  60. Vandermosten M, Boets B, Poelmans H, Sunaert S, Wouters J, Ghesquiere P (2012) A tractography study in dyslexia: neuroanatomic correlates of orthographic, phonological and speech processing. Brain 135(Pt 3):935–948.  https://doi.org/10.1093/brain/awr363 CrossRefPubMedGoogle Scholar
  61. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl P, Mori S (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36(3):630–644.  https://doi.org/10.1016/j.neuroimage.2007.02.049 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wan CY, Schlaug G (2010) Neural pathways for language in autism: the potential for music-based treatments. Future Neurol 5(6):797–805CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wang X, Peng G (2014) Phonological processing in Mandarin speakers with congenital amusia. J Acoust Soc Am 136(6):3360.  https://doi.org/10.1121/1.4900559 CrossRefPubMedGoogle Scholar
  64. Wang R, Benner T, Sorensen A, Wedeen V (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. Proc Intl Soc Mag Reson Med 3720Google Scholar
  65. Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D’Arceuil H, de Crespigny AJ (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage 41(4):1267–1277.  https://doi.org/10.1016/j.neuroimage.2008.03.036 CrossRefPubMedGoogle Scholar
  66. Wildgruber D, Ackermann H, Kreifelts B, Ethofer T (2006) Cerebral processing of linguistic and emotional prosody: fMRI studies. Progress Brain Res 156:249–268.  https://doi.org/10.1016/S0079-6123(06)56013-3 CrossRefGoogle Scholar
  67. Yang WX, Feng J, Huang WT, Zhang CX, Nan Y (2014) Perceptual pitch deficits coexist with pitch production difficulties in music but not Mandarin speech. Front Psychol 4:1024.  https://doi.org/10.3389/fpsyg.2013.01024 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yeatman JD, Dougherty RF, Rykhlevskaia E, Sherbondy AJ, Deutsch GK, Wandell BA, Ben-Shachar M (2011) Anatomical properties of the arcuate fasciculus predict phonological and reading skills in children. J Cogn Neurosci 23(11):3304–3317.  https://doi.org/10.1162/jocn_a_00061 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Yeatman JD, Dougherty RF, Ben-Shachar M, Wandell BA (2012) Development of white matter and reading skills. Proc Natl Acad Sci USA 109(44):E3045–E3053.  https://doi.org/10.1073/pnas.1206792109 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Zalesky A, Fornito A, Cocchi L, Gollo LL, van den Heuvel MP, Breakspear M (2016) Connectome sensitivity or specificity: which is more important? Neuroimage 142:407–420.  https://doi.org/10.1016/j.neuroimage.2016.06.035 CrossRefPubMedGoogle Scholar
  71. Zatorre RJ, Baum SR (2012) Musical melody and speech intonation: singing a different tune. PLoS Biol 10(7):e1001372.  https://doi.org/10.1371/journal.pbio.1001372 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Zhao Y, Chen X, Zhong S, Cui Z, Gong G, Dong Q, Nan Y (2016) Abnormal topological organization of the white matter network in Mandarin speakers with congenital amusia. Sci Rep 6:26505.  https://doi.org/10.1038/srep26505 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xizhuo Chen
    • 1
  • Yanxin Zhao
    • 1
  • Suyu Zhong
    • 1
  • Zaixu Cui
    • 1
  • Jiaqi Li
    • 1
  • Gaolang Gong
    • 1
  • Qi Dong
    • 1
  • Yun Nan
    • 1
  1. 1.State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain ResearchBeijing Normal UniversityBeijingPeople’s Republic of China

Personalised recommendations