Top

Published in:

01-05-2018 | Original Article

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

Authors: Xizhuo Chen, Yanxin Zhao, Suyu Zhong, Zaixu Cui, Jiaqi Li, Gaolang Gong, Qi Dong, Yun Nan

Published in: Brain Structure and Function | Issue 4/2018

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.

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 PubMedPubMedCentral

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 PubMed

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 PubMedPubMedCentral

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

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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

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):207–222CrossRefPubMed

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 CrossRefPubMed

Gong Y, Cai T (1993) Manual of Chinese revised Wechsler intelligence scale for children. Hunan Atlas Publishing House, Changsha

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 CrossRefPubMedPubMedCentral

Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8(5):393–402. https://doi.org/10.1038/nrn2113 CrossRefPubMed

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 PubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 PubMed

Liberman AM, Harris KS, Hoffman HS, Griffith BC (1957) The discrimination of speech sounds within and across phoneme boundaries. J Exp Psychol 54(5):358–368CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113CrossRefPubMed

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 CrossRefPubMed

Pardo JS (2006) On phonetic convergence during conversational interaction. J Acoust Soc Am 119(4):2382–2393CrossRefPubMed

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 CrossRef

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]CrossRefPubMed

Peretz I, Champod AS, Hyde K (2003) Varieties of musical disorders. The montreal battery of evaluation of amusia. Ann N Y Acad Sci 999:58–75CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

Wan CY, Schlaug G (2010) Neural pathways for language in autism: the potential for music-based treatments. Future Neurol 5(6):797–805CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 3720

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMedPubMedCentral

Title: The lateralized arcuate fasciculus in developmental pitch disorders among mandarin amusics: left for speech and right for music
Authors: Xizhuo Chen
Yanxin Zhao
Suyu Zhong
Zaixu Cui
Jiaqi Li
Gaolang Gong
Qi Dong
Yun Nan
Publication date: 01-05-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1608-2

At a glance: The STEP trials

Springer Medicine

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

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

Comparing brain activity patterns during spontaneous exploratory and cue-instructed learning using single photon-emission computed tomography (SPECT) imaging of regional cerebral blood flow in freely behaving rats

Plasticity in deep and superficial white matter: a DTI study in world class gymnasts

Different neural substrates for precision stepping and fast online step adjustments in youth

Changes in neocortical and hippocampal microglial cells during hibernation

Vascular pattern of the dentate gyrus is regulated by neural progenitors

Neuronal density and proportion of interneurons in the associative, sensorimotor and limbic human striatum