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Interhemispheric transcallosal connectivity between the left and right planum temporale predicts musicianship, performance in temporal speech processing, and functional specialization

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Abstract

Currently, there is strong evidence showing that musicianship favours functional and structural changes of the left planum temporale (PT), and that these cortical reorganizations facilitate the discrimination of temporal speech cues. Based on the proposition of a division of labour between the left and right PT, here we postulated that the musicians’ advantage in processing temporal speech cues and PT specialization origin, at least in part, from increased white matter connectivity between the two auditory-related cortices. In particular, we assume that increased transcallosal PT connectivity might promote functional specialization and asymmetry of homotopic brain regions. With this purpose in mind, we applied diffusion tensor imaging and compared axial diffusivity (AD), radial diffusivity (RD), and fractional anisotropy (FA) of the interhemispheric connection between the left and right PT in thirteen musicians and 13 nonmusicians. Furthermore, in the form of an addendum, we integrated cortical surface area values and blood oxygenation level dependent (BOLD) responses of the left PT that were collected in the context of two previous studies conducted with the same sample of subjects. Our results indicate increased connectivity between the left and right PT in musicians compared to nonmusicians, as indexed by reduced mean RD. We did not find significant between-group differences in FA and AD. Most notably, RD was related to the performance in the phonetic categorization task, musical aptitudes, as well as to BOLD responses in the left PT. Hence, we provide first evidence for a relationship between PT connectivity, musicianship, and phonetic categorization.

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References

  • Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus-callosum. Brain Res 598:143–153

    Article  PubMed  CAS  Google Scholar 

  • Alexander AL, Lee JE, Lazar M, Field AS (2007) Diffusion tensor imaging of the brain. Neurotherapeutics 4:316–329

    Article  PubMed Central  PubMed  Google Scholar 

  • Annett M (1970) A classification of hand preference by association analysis. Br J Psychol 61:303–321

    Article  PubMed  CAS  Google Scholar 

  • Bartsch AJ, Biller A, Homola GA (2009) Tractography for surgical targets. In: Johansen-Berg H, Behrens TEJ (eds) Diffusion MRI: from quantitative measurement to in vivo neuroanatomy. Academic Press, Amsterdan

    Google Scholar 

  • Bartzokis G, Beckson M, Lu PH, Nuechterlein KH, Edwards N, Mintz J (2001) Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. Arch Gen Psychiatry 58:461–465

    Article  PubMed  CAS  Google Scholar 

  • Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–455

    Article  PubMed  Google Scholar 

  • Beaulieu C (2009) The biological basis of diffusion anisotropy. In: Johansen-Berg H, Behrens TEJ (eds) Diffusion MRI: from quantitative measurement to in vivo neuroanatomy. Academic Press, Amsterdam

    Google Scholar 

  • Beaulieu C, Does MD, Snyder RE, Allen PS (1996) Changes in water diffusion due to wallerian degeneration in peripheral nerve. Magn Reson Med 36:627–631

    Article  PubMed  CAS  Google Scholar 

  • Belin P, Zilbovicius M, Crozier S, Thivard L, Fontaine A, Masure MC, Samson Y (1998) Lateralization of speech and auditory temporal processing. J Cogn Neurosci 10(4):536–540

    Article  PubMed  CAS  Google Scholar 

  • Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullen F (2005) Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8:1148–1150

    Article  PubMed  CAS  Google Scholar 

  • Bermudez P, Lerch JP, Evans AC, Zatorre RJ (2009) Neuroanatomical correlates of musicianship as revealed by cortical thickness and voxel-based morphometry. Cereb Cortex 19:1583–1596

    Article  PubMed  Google Scholar 

  • Brechmann A, Scheich H (2005) Hemispheric shifts of sound representation in auditory cortex with conceptual listening. Cereb Cortex 15:578–587

    Article  PubMed  Google Scholar 

  • Burgel U, Schormann T, Schleicher A, Zilles K (1999) Mapping of histologically identified long fiber tracts in human cerebral hemispheres to the MRI volume of a reference brain: position and spatial variability of the optic radiation. Neuroimage 10:489–499

    Article  PubMed  CAS  Google Scholar 

  • Burgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29:1092–1105

    Article  PubMed  Google Scholar 

  • Chao YP, Cho KH, Yeh CH, Chou KH, Chen JH, Lin CP (2009) Probabilistic topography of human corpus callosum Using cytoarchitectural parcellation and high angular resolution diffusion imaging tractography. Hum Brain Mapp 30:3172–3187

    Article  PubMed  Google Scholar 

  • Ellis RJ, Bruijn B, Norton AC, Einner E, Schlaug G (2013) Training-mediated leftward asymmetries during music processing: A cross-sectional and longitudinal fMRI analysis. Neuroimage 75:97–107. doi:10.1016/j.neuroimage.2013.02.045

    Article  PubMed Central  PubMed  Google Scholar 

  • Elmer S, Meyer M, Marrama L, Jancke L (2011) Intensive language training and attention modulate the involvement of fronto-parietal regions during a non-verbal auditory discrimination task. Eur J Neurosci 34:165–175

    Article  PubMed  Google Scholar 

  • Elmer S, Meyer M, Jancke L (2012) Neurofunctional and behavioral correlates of phonetic and temporal categorization in musically trained and untrained subjects. Cereb Cortex 22:650–658

    Article  PubMed  Google Scholar 

  • Elmer S, Hänggi J, Meyer M, Jäncke L (2013) Increased cortical surface area of the left planum temporale in musicians facilitates the categorization of phonetic and temporal speech sounds. Cortex. doi:10.1016/j.cortex.2013.03.007

    PubMed  Google Scholar 

  • Fedorenko E, McDermott JH, Norman-Haignere S, Kanwisher N (2012) Sensitivity to musical structure in the human brain. J Neurophysiol 108(12):3289–3300

    Article  PubMed Central  PubMed  Google Scholar 

  • Friederici AD, von Cramon DY, Kotz SA (2007) Role of the corpus callosum in speech comprehension: interfacing syntax and prosody. Neuron 53:135–145

    Article  PubMed  CAS  Google Scholar 

  • Galaburda AM (1991) Asymmetries of cerebral neuroanatomy. Ciba Found Symp 162:219–233

    PubMed  CAS  Google Scholar 

  • Galaburda AM, Rosen GD, Sherman GF (1990) Individual variability in cortical organization: its relationship to brain laterality and implications to function. Neuropsychologia 28:529–546

    Article  PubMed  CAS  Google Scholar 

  • Geschwind N, Levitsky W (1968) Human brain: left–right asymmetries in temporal speech regions. Science 161:186–187

    Article  PubMed  CAS  Google Scholar 

  • Giraud AL, Kleinschmidt A, Poeppel D, Lund TE, Frackowiak RSJ, Laufs H (2007) Endogenous cortical rhythms determine cerebral specialization for speech perception and production. Neuron 56:1127–1134

    Article  PubMed  CAS  Google Scholar 

  • Gordon EE (1989) Manual for the advanced measures of music education. G.I.A. Publications, Inc, Chicago

    Google Scholar 

  • Griffiths TD, Warren JD (2002) The planum temporale as a computational hub. Trends Neurosci 25:348–353

    Article  PubMed  CAS  Google Scholar 

  • Halwani GF, Loiu P, Rüber T, Schlaug G (2011) Effects of practice and experience on the arcuate fasciculus: comparing singers, instrumentalists, and non-musicians. Front Psychol. doi:10.3389/fpsyg.2011.00156

    PubMed Central  PubMed  Google Scholar 

  • Harasty J, Seldon L, Chan P, Halliday G, Harding A (2001) The left human speech-processing cortex is thinner but longer than the right. Aust J Psychol 53:180

    Google Scholar 

  • Hofer S, Frahm J (2006) Topography of the human corpus callosum revisited: comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage 32:989–994

    Article  PubMed  Google Scholar 

  • Hofstetter S, Tavor I, Moryosef ST, Asaf Y (2013) Short-term learning induces white matter plasticity in the fornix. J Neurosci 33:12844–12850

    Article  PubMed  CAS  Google Scholar 

  • Hyde KL, Lerch J, Norton A, Forgeard M, Winner E, Evans AC, Schlaug G (2009) Musical training shapes structural brain development. J Neurosci 29:3019–3025

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Imfeld A, Oechslin MS, Meyer M, Loenneker T, Jancke L (2009) White matter plasticity in the corticospinal tract of musicians: a diffusion tensor imaging study. Neuroimage 46:600–607

    Article  PubMed  Google Scholar 

  • Jancke L, Shah NJ (2002) Does dichotic listening probe temporal lobe functions? Neurology 58:736–743

    Article  PubMed  CAS  Google Scholar 

  • Jäncke L, Steinmetz H (2003) Anatomical brain asymmetries and their relevance for functional asymmetries. In: Hugdahl K, Davidson RJ (eds) The asymmetical brain. MIT Press, Cambridge, pp 187–229

    Google Scholar 

  • Jancke L, Wustenberg T, Scheich H, Heinze HJ (2002) Phonetic perception and the temporal cortex. Neuroimage 15:733–746

    Article  PubMed  CAS  Google Scholar 

  • Josse G, Tzourio-Mazoyer N (2004) Hemispheric specialization for language. Brain Res Rev 44:1–12

    Article  PubMed  Google Scholar 

  • Josse G, Mazoyer B, Crivello F, Tzourio-Mazoyer N (2003) Left planum temporale: an anatomical marker of left hemispheric specialization for language comprehension. Cogn Brain Res 18:1–14

    Article  Google Scholar 

  • Keenan JP, Thangaraj V, Halpern AR, Schlaug G (2001) Absolute pitch and planum temporale. Neuroimage 14:1402–1408

    Article  PubMed  CAS  Google Scholar 

  • Klawiter EC, Schmidt RE, Trinkaus K, Liang HF, Budde MD, Naismith RT, Song SK, Cross AH, Benzinger TL (2011) Radial diffusivity predicts demyelination in ex vivo multiple sclerosis spinal cords. Neuroimage 55:1454–1460

    Article  PubMed Central  PubMed  Google Scholar 

  • Kraus N, Chandrasekaran B (2010) Music training for the development of auditory skills. Nat Rev Neurosci 11(8):599–605

    Article  PubMed  CAS  Google Scholar 

  • Kühnis J, Elmer S, Meyer M, Jäncke L (2013) The encoding of vowels and temporal speech cues in the auditory cortex of professional musicians: an EEG study. Neuropsychologia. doi:10.1016/j.neuropsychologia.2013.04.007

    PubMed  Google Scholar 

  • Kühnis J, Elmer S, Jäncke L (2014) Auditory evoked responses in musicians during passive vowel listening are modulated by functional connectivity between bilateral auditory-related brain regions. J Cogn Neurosci 4:12

    Google Scholar 

  • Lee DJ, Chen Y, Schlaug G (2003) Corpus callosum: musician and gender effects. Neuroreport 14:205–209

    Article  PubMed  Google Scholar 

  • Lehrl S, Fischer B (1992) Kurztest für allgemeine Basisgrössen der Informationsverarbeitung (KAI), vol 3. Aufl. Vless, Ebersberg

  • Lisker L, Abramson AS (1964) A cross-language study of voicing in initial stops: acoustical measurements. Word J Int Linguist Assoc 20:384–422

    Google Scholar 

  • Lisker L, Abramson AS (1967) Some effects of context on voice onset time in english stops. Lang Speech 10:1–28

    PubMed  CAS  Google Scholar 

  • Loui P, Li HC, Hohmann A, Schlaug G (2011) Enhanced cortical connectivity in absolute pitch musicians: a model for local hyperconnectivity. J Cogn Neurosci 23:1015–1026

    Article  PubMed Central  PubMed  Google Scholar 

  • Luders E, Gaser C, Jancke L, Schlaug G (2004) A voxel-based approach to gray matter asymmetries. Neuroimage 22:656–664

    Article  PubMed  CAS  Google Scholar 

  • Merzenich MM, Jenkins WM, Johnston P, Schreiner C, Miller SL, Tallal P (1996) Temporal processing deficits of language-learning impaired children ameliorated by training. Science 271(5245):77–81

    Article  PubMed  CAS  Google Scholar 

  • Meyer M (2008) Functions of the left and right posterior temporal lobes during segmental and suprasegmental speech perception. Zeitschrift fur Neuropsychologie 19:101–115

    Article  Google Scholar 

  • Meyer M, Elmer S, Jancke L (2012) Musical expertise induces neuroplasticity of the planum temporale. Neurosci Music Iv: Learn Memory 1252:116–123

    Google Scholar 

  • Mori S, Zhang JY (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–539

    Article  PubMed  CAS  Google Scholar 

  • Munte TF, Altenmuller E, Jancke L (2002) The musician’s brain as a model of neuroplasticity. Nat Rev Neurosci 3:473–478

    PubMed  Google Scholar 

  • Ohnishi T, Matsuda H, Asada T, Aruga M, Hirakata M, Nishikawa M, Katoh A, Imabayashi E (2001) Functional anatomy of musical perception in musicians. Cereb Cortex 11:754–760

    Article  PubMed  CAS  Google Scholar 

  • Ott CGM, Langer N, Oechslin MS, Meyer M, Jäncke L (2012) Processing of voiced and unvoiced acoustic stimuli in musicians. Front Psychol 2:195. doi:10.3389/fpsyg.2011.00195

    Google Scholar 

  • Ozturk AH, Tascioglu B, Aktekin M, Kurtoglu Z, Erden I (2002) Morphometric comparison of the human corpus callosum in professional musicians and non-musicians by using in vivo magnetic resonance imaging. J Neuroradiol 29:29–34

    PubMed  Google Scholar 

  • Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix L, Virta A, Basser P (2001) Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 13:1174–1185

    Article  PubMed  CAS  Google Scholar 

  • Poeppel D (2003) The analysis of speech in different temporal integration windows: cerebral lateralization as ‘asymmetric sampling in time’. Speech Commun 41:245–255

    Article  Google Scholar 

  • Price CJ (2010) The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci 1191:62–88

    Article  PubMed  Google Scholar 

  • Rosas HD, Lee SY, Bender AC, Zaleta AK, Vangel M, Yu P, Fischl B, Pappu V, Onorato C, Cha JH, Salat DH, Hersch SM (2010) Altered white matter microstructure in the corpus callosum in Huntington’s disease: implications for cortical “disconnection”. Neuroimage 49:2995–3004

    Article  PubMed  Google Scholar 

  • Rosen GD, Sherman GF, Galaburda AM (1989) Interhemispheric connections differ between symmetrical and asymmetrical brain-regions. Neuroscience 33:525–533

    Article  PubMed  CAS  Google Scholar 

  • Särkämö T, Tervaniemi M, Laitinen S, Numminen A, Kurki M, Johnson JK, Rantanen P (2014) Cognitive, emotional, and social benefits of regular musical activities in early dementia: randomized controlled study. Gerontologist 54(4):634–650

    Article  PubMed  Google Scholar 

  • Schlaug G, Jancke L, Huang YX, Staiger JF, Steinmetz H (1995a) Increased corpus-callosum size in musicians. Neuropsychologia 33:1047

    Article  PubMed  CAS  Google Scholar 

  • Schlaug G, Jancke L, Huang YX, Steinmetz H (1995b) In-vivo evidence of structural brain asymmetry in musicians. Science 267:699–701

    Article  PubMed  CAS  Google Scholar 

  • Schlaug G, Forgeard M, Zhu L, Norton A, Norton A, Winner E (2009) Training-induced neuroplasticity in young children. Neurosci Music Iii 1169:205–208

    Google Scholar 

  • Schmithorst VJ, Wilke M (2002) Differences in white matter architecture between musicians and non-musicians: a diffusion tensor imaging study. Neurosci Lett 321:57–60

    Article  PubMed  CAS  Google Scholar 

  • Seldon HL (1981a) Structure of human Auditory-cortex. 1 cytoarchitectonics and dendritic distributions. Brain Res 229:277–294

    Article  PubMed  CAS  Google Scholar 

  • Seldon HL (1981b) Structure of human auditory-cortex. 2. Axon distributions and morphological correlates of speech-perception. Brain Res 229:295–310

    Article  PubMed  CAS  Google Scholar 

  • Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primarily temporal cues. Science 270:303–304

    Article  PubMed  CAS  Google Scholar 

  • Shapleske J, Rossell SL, Woodruff PW, David AS (1999) The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Brain Res Rev 29(1):26–49

    Article  PubMed  CAS  Google Scholar 

  • Simper R, Walker MA, Black G, Di Rosa E, Crow TJ, Chance SA (2011) The relationship between callosal axons and cortical neurons in the planum temporale: alterations in schizophrenia. Neurosci Res 71(4):405–410

    Article  PubMed  CAS  Google Scholar 

  • Sinai A, Pratt H (2003) High-resolution time course of hemispheric dominance revealed by low-resolution electromagnetic tomography. Clin Neurophysiol 114:1181–1188

    Article  PubMed  Google Scholar 

  • Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155

    Article  PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang YY, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219

    Article  PubMed  Google Scholar 

  • Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436

    Article  PubMed  Google Scholar 

  • Steele CJ, Bailey JA, Zatorre RJ, Penhune VB (2013) Early musical training and white-matter plasticity in the corpus callosum: evidence for a sensitive period. J Neurosci 33:1282–1290

    Article  PubMed  CAS  Google Scholar 

  • Steinmetz H (1996) Structure, function and cerebral asymmetry: in vivo morphometry of the planum temporale. Neurosci Biobehav Rev 20:587–591

    Article  PubMed  CAS  Google Scholar 

  • Steinmetz H, Volkmann J, Jancke L, Freund HJ (1991) Anatomical left-right asymmetry of language-related temporal cortex is different in left-handers and right-handers. Ann Neurol 29:315–319

    Article  PubMed  CAS  Google Scholar 

  • Sun SW, Liang HF, Cross AH, Song SK (2008) Evolving Wallerian degeneration after transient retinal ischemia in mice characterized by diffusion tensor imaging. Neuroimage 40:1–10

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tournier J, Yeh CH, Calamante F, Cho KH, Conelly A (2008) resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 42(2):617–625

    Article  PubMed  Google Scholar 

  • Tzourio N, Crivello F, Mellet E, Nkanga-Ngila B, Mazoyer B (1998a) Functional anatomy of dominance for speech comprehension in left handers vs right handers. Neuroimage 8:1–16

    Article  PubMed  CAS  Google Scholar 

  • Tzourio N, Nkanga-Ngila B, Mazoyer B (1998b) Left planum temporale surface correlates with functional dominance during story listening. Neuroreport 9:829–833

    Article  PubMed  CAS  Google Scholar 

  • Uitenbroek DG (1997) SISA Binomial

  • Warrier C, Wong P, Penhune V, Zatorre R, Parrish T, Abrams D, Kraus N (2009) Relating structure to function: heschl’s gyrus and acoustic processing. J Neurosci 29(1):61–69

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Westerhausen R, Gruner R, Specht K, Hugdahl K (2009) Functional relevance of interindividual differences in temporal lobe callosal pathways: a DTI tractography study. Cereb Cortex 19:1322–1329

    Article  PubMed  Google Scholar 

  • Wheeler-Kingshott CA, Cercignani M (2009) About “axial” and “radial” diffusivities. Magn Reson Med 61(5):1255–1260

    Article  PubMed  Google Scholar 

  • Zaehle T, Wustenberg T, Meyer M, Jancke L (2004) Evidence for rapid auditory perception as the foundation of speech processing: a sparse temporal sampling fMRI study. Eur J Neurosci 20:2447–2456

    Article  PubMed  CAS  Google Scholar 

  • Zaehle T, Geiser E, Alter K, Jancke L, Meyer M (2008) Segmental processing in the human auditory dorsal stream. Brain Res 1220:179–190

    Article  PubMed  CAS  Google Scholar 

  • Zatorre RJ, Belin P (2001) Spectral and temporal processing in human auditory cortex. Cereb Cortex 11(10):946–953

    Article  PubMed  CAS  Google Scholar 

  • Zatorre RJ, Fields RD, Johansen-Berg H (2012) Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci 15:528–536

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Swiss National Foundation (SNF, Grant No. 320030-120661 and Grant No. 4-62341-05 to LJ).

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The authors declare that they have no competing interests.

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Authors and Affiliations

  1. Division of Neuropsychology, Institute of Psychology, University of Zurich, Zurich, Switzerland

    Stefan Elmer, Jürgen Hänggi & Lutz Jäncke

  2. Center for Integrative Human Physiology, University of Zurich, Zurich, Switzerland

    Lutz Jäncke

  3. International Normal Aging and Plasticity Imaging Center (INAPIC), University of Zurich, Zurich, Switzerland

    Lutz Jäncke

  4. University Research Priority Program (URPP) “Dynamic of Healthy Aging”, University of Zurich, Zurich, Switzerland

    Lutz Jäncke

  5. Department of Special Education, King Abdulaziz University, Jeddah, Saudi Arabia

    Lutz Jäncke

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  1. Stefan Elmer
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Correspondence to Stefan Elmer.

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S. Elmer and J. Hänggi contributed equally to this study.

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Elmer, S., Hänggi, J. & Jäncke, L. Interhemispheric transcallosal connectivity between the left and right planum temporale predicts musicianship, performance in temporal speech processing, and functional specialization. Brain Struct Funct 221, 331–344 (2016). https://doi.org/10.1007/s00429-014-0910-x

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