The robust and independent nature of structural STS asymmetries

  • Jonathan S. BainEmail author
  • Shir Filo
  • Aviv A. Mezer
Original Article


The superior temporal sulcus (STS) is an important region for speech comprehension. The greater language network is known to exhibit asymmetries in both structure and function, and consistent with that theory are reports of STS structural asymmetry in MRI-based, morphological measures such as mean thickness and sulcal depth. However, it is not known how these individual STS structural asymmetries relate to each other, or how they interact with the broader language asymmetry that manifests in other brain regions. In this study, we assess the interrelations of STS asymmetries in the human brain in vivo, using four independent datasets to validate our findings. For morphological measurements, we identify STS laterality effects consistent between our datasets and with the literature: leftward for surface area, and rightward for sulcal depth and mean thickness. We then add two more measurements of STS asymmetry: in T1, a quantitative index of the tissue’s underlying biophysical properties; and in the projections to the STS from the arcuate fasciculus, a left-lateralized white-matter bundle that connects temporal regions (including STS) with frontal regions (including Broca’s area). For these two new measurements, we identify no effect for T1 and a leftward effect for arcuate projections. We then test for correlations between these STS asymmetries, and find associations mainly between measurements of the same type (e.g., two morphological measurements). Finally, we ask if STS asymmetry is preferentially related to Broca asymmetry, as these are both important language regions and connected via the arcuate fasciculus. Using a linear model with cross-validation, we find that random regions are as successful as Broca’s area in predicting STS, and no indication of a hypothesized leftward asymmetry. We conclude that although these different STS asymmetries are robust across datasets, they are not trivially related to each other, suggesting different biological or imaging sources for different aspects of STS lateralities.


Arcuate fasciculus Asymmetry Broca’s area Language Replication 



The authors thank B. Wandell for data collection, which was supported by the Weston Havens foundation, the National Science Foundation (BCS1228397) and National Institutes of Health (EY015000); Y. Grodzinsky and G. Agmon for additional data collection; and A. Erramuzpe and R. Schurr for their constructive comments and suggestions.

Author contributions

SF collected data; JSB and AAM performed analysis and wrote the manuscript.


This work was supported by the United States–Israel Binational Science Foundation (BCS1551330 to AAM); the Israel Science Foundation (0399306 to AAM).

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Research involving human participants and/or animals

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

429_2019_1952_MOESM1_ESM.docx (648 kb)
Supplementary material 1 (DOCX 647 kb)


  1. Amunts K, Schleicher A, Burgel U, Mohlberg H, Uylings HB, Zilles K (1999) Broca’s region revisited: cytoarchitecture and intersubject variability. J Comp Neurol 412(2):319–341CrossRefGoogle Scholar
  2. Amunts K, Schleicher A, Ditterich A, Zilles K (2003) Broca’s region: cytoarchitectonic asymmetry and developmental changes. J Comp Neurol 465(1):72–89. CrossRefGoogle Scholar
  3. Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage 54(3):2033–2044. CrossRefGoogle Scholar
  4. Bain JS, Yeatman JD, Schurr R, Rokem A, Mezer AA (2019) Evaluating arcuate fasciculus laterality measurements across dataset and tractography pipelines. Hum Brain Mapp 40(13):3695–3711. Google Scholar
  5. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15(7–8):435–455. CrossRefGoogle Scholar
  6. Bodin C, Takerkart S, Belin P, Coulon O (2018) Anatomo-functional correspondence in the superior temporal sulcus. Brain Struct Funct 223(1):221–232. CrossRefGoogle Scholar
  7. Broca P (1865) Sur Le Siège de La Faculté Du Langage Articulé. Bulletins de La Société d’anthropologie de Paris 1(6):377–393. CrossRefGoogle Scholar
  8. Carey D, Caprini F, Allen M, Lutti A, Weiskopf N, Rees G, Callaghan MF, Dick F (2018) Quantitative MRI provides markers of intra-, inter-regional, and age-related differences in young adult cortical microstructure. NeuroImage 182(15):429–440. CrossRefGoogle Scholar
  9. Catani M, Allin MPG, 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. CrossRefGoogle Scholar
  10. Cercignani M, D NG, Tofts Paul (eds) (2018) Quantitative MRI of the brain: principles of physical measurement, 2nd edn. CRC Press, LondonGoogle Scholar
  11. Chang L-C, Koay CG, Basser PJ, Pierpaoli C (2008) Linear least-squares method for unbiased estimation of T1 from SPGR signals. Magn Reson Med 60(2):496–501. CrossRefGoogle Scholar
  12. Croxson PL, Forkel SJ, Cerliani L, de Schotten MT (2018) Structural variability across the primate brain: a cross-species comparison. Cereb Cortex 28(11):1–13. CrossRefGoogle Scholar
  13. Daducci A, Dal Palú A, Descoteaux M, Thiran J-P (2016) Microstructure informed tractography: pitfalls and open challenges. Front Neurosci. Google Scholar
  14. Dehaene S, Dupoux E, Mehler J, Cohen L, Paulesu E, Perani D, van de Moortele PF, Lehéricy S, Le Bihan D (1997) Anatomical variability in the cortical representation of first and second language. NeuroReport 8(17):3809–3815CrossRefGoogle Scholar
  15. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31(3):968–980. CrossRefGoogle Scholar
  16. DeWitt I, Rauschecker JP (2013) Wernicke’s area revisited: parallel streams and word processing. Brain Lang 127(2):181–191. CrossRefGoogle Scholar
  17. Filo S, Shtangel O, Salamon N, Kol A, Weisinger B, Shifman S, Mezer AA (2019) Disentangling molecular alterations from water-content changes in the aging human brain using quantitative MRI. Nat Commun 10(1):3403CrossRefGoogle Scholar
  18. Geschwind N (1970) The organization of language and the brain. Science 170(3961):940–944CrossRefGoogle Scholar
  19. Geschwind N, Levitsky W (1968) Human brain: left–right asymmetries in temporal speech region. Science 161(3837):186–187. CrossRefGoogle Scholar
  20. Glasser MF, Sotiropoulos SN, Wilson JA, Coalson TS, Fischl B, Andersson JL, Xu J et al (2013) The minimal preprocessing pipelines for the Human Connectome Project. NeuroImage 80(Suppl C):105–124. CrossRefGoogle Scholar
  21. Hagoort P (2014) Nodes and networks in the neural architecture for language: Broca’s region and beyond. Curr Opin Neurobiol 28:136–141. CrossRefGoogle Scholar
  22. Hickok G, Poeppel D (2016) Neural basis of speech perception, Chapter 25. In: Hickok G, Small SL (eds) Neurobiology of language. Academic Press, San Diego, pp 299–310. CrossRefGoogle Scholar
  23. Hilgetag CC, Barbas H (2006) Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2(3):e22. CrossRefGoogle Scholar
  24. Hutsler JJ (2003) The specialized structure of human language cortex: pyramidal cell size asymmetries within auditory and language-associated regions of the temporal lobes. Brain Lang Underst Lang 86(2):226–242. CrossRefGoogle Scholar
  25. Hutsler JJ, Galuske RAW (2003) Hemispheric asymmetries in cerebral cortical networks. Trends Neurosci 26(8):429–435. CrossRefGoogle Scholar
  26. Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage 73(June):239–254. CrossRefGoogle Scholar
  27. Keller SS, Crow T, Foundas A, Amunts K, Roberts N (2009) Broca’s area: nomenclature, anatomy, typology and asymmetry. Brain Lang 109(1):29–48. CrossRefGoogle Scholar
  28. Kong X-Z, Mathias CR, Guadalupe T, ENIGMA Laterality Working Group, Glahn DC, Franke B, Crivello F et al (2018) Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA consortium. Proc Natl Acad Sci 115(22):E5154–E5163. CrossRefGoogle Scholar
  29. Le Guen Y, Leroy F, Auzias G, Riviere D, Grigis A, Mangin J-F, Coulon O, Dehaene-Lambertz G, Frouin V (2018) The chaotic morphology of the left superior temporal sulcus is genetically constrained. NeuroImage 174(July):297–307. CrossRefGoogle Scholar
  30. Lebois A (2014) Brain microstructure mapping using quantitative and diffusion MRI. PhD thesis, Université Paris Sud-Paris XI.
  31. Leroy F, Cai Q, Bogart SL, Dubois J, Coulon O, Monzalvo K, Fischer C et al (2015) New human-specific brain landmark: the depth asymmetry of superior temporal sulcus. Proc Natl Acad Sci USA 112(4):1208–1213. CrossRefGoogle Scholar
  32. Lopez-Barroso D, Catani M, Ripollés P, Dell’Acqua F, Rodríguez-Fornells A, de Diego-Balaguer R (2013) Word learning is mediated by the left arcuate fasciculus. Proc Natl Acad Sci 110(32):13168–13173. CrossRefGoogle Scholar
  33. Margulies DS, Ghosh SS, Goulas A, Falkiewicz M, Huntenburg JM, Langs G, Bezgin G et al (2016) Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc Natl Acad Sci 113(44):12574–12579. CrossRefGoogle Scholar
  34. McGettigan C, Faulkner A, Altarelli I, Obleser J, Baverstock H, Scott SK (2012) Speech comprehension aided by multiple modalities: behavioural and neural interactions. Neuropsychologia 50(5):762–776. CrossRefGoogle Scholar
  35. Meyer L, Obleser J, Anwander A, Friederici AD (2012) Linking ordering in broca’s area to storage in left temporo-parietal regions: the case of sentence processing. NeuroImage 62(3):1987–1998. CrossRefGoogle Scholar
  36. Mezer A, Yeatman JD, Stikov N, Kay KN, Cho N-J, Dougherty RF, Perry ML et al (2013) Quantifying the local tissue volume and composition in individual brains with magnetic resonance imaging. Nat Med 19(12):1667–1672CrossRefGoogle Scholar
  37. Mezer A, Rokem A, Berman S, Hastie T, Wandell BA (2016) Evaluating quantitative proton-density-mapping methods. Hum Brain Mapp 37(10):3623–3635. CrossRefGoogle Scholar
  38. Nucifora PGP, Verma R, Melhem ER, Gur RE, Gur RC (2005) Leftward asymmetry in relative fiber density of the arcuate fasciculus. NeuroReport 16(8):791–794CrossRefGoogle Scholar
  39. Pestilli F, Yeatman JD, Rokem A, Kay KN, Wandell BA (2014) Evaluation and statistical inference for living connectomes. Nat Methods 11(10):1058–1063. CrossRefGoogle Scholar
  40. Poeppel D, Hickok G (2004) Towards a new functional anatomy of language. Cognition 92(1–2):1–12. CrossRefGoogle Scholar
  41. Popper K (1962) The logic of scientific discovery, revised edition. Hutchinson, ParisGoogle Scholar
  42. Rampinini AC, Handjaras G, Leo A, Cecchetti L, Ricciardi E, Marotta G, Pietrini P (2017) Functional and spatial segregation within the inferior frontal and superior temporal cortices during listening, articulation imagery, and production of vowels. Sci Rep 7(1):17029. CrossRefGoogle Scholar
  43. Reese TG, Heid O, Weisskoff RM, Wedeen VJ (2003) Reduction of Eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn Reson Med 49(1):177–182. CrossRefGoogle Scholar
  44. Rilling JK (2014) Comparative primate neurobiology and the evolution of brain language systems. Curr Opin Neurobiol 28:10–14. CrossRefGoogle Scholar
  45. Rilling JK, Glasser MF, Jbabdi S, Andersson J, Preuss TM (2012) Continuity, divergence, and the evolution of brain language pathways. Front Evol Neurosci. Google Scholar
  46. Rogalsky C, Hickok G (2010) The role of Broca’s area in sentence comprehension. J Cogn Neurosci 23(7):1664–1680. CrossRefGoogle Scholar
  47. Schell M, Zaccarella E, Friederici AD (2017) Differential cortical contribution of syntax and semantics: an FMRI study on two-word phrasal processing. Cortex 96(Suppl C):105–120. CrossRefGoogle Scholar
  48. Schenker NM, Hopkins WD, Spocter MA, Garrison AR, Stimpson CD, Erwin JM, Hof PR, Sherwood CC (2010) Broca’s area homologue in chimpanzees (Pan troglodytes): probabilistic mapping, asymmetry, and comparison to humans. Cereb Cortex (New York, NY) 20(3):730–742. Google Scholar
  49. Setsompop K, Fan Q, Stockmann J, Bilgic B, Huang S, Cauley SF, Nummenmaa A et al (2018) High-resolution in vivo diffusion imaging of the human brain with generalized slice dithered enhanced resolution: simultaneous multislice (GSlider-SMS). Magn Reson Med 79(1):141–151. CrossRefGoogle Scholar
  50. Smith RE, Tournier J-D, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. NeuroImage 62(3):1924–1938. CrossRefGoogle Scholar
  51. Stuber C, Morawski M, Schafer A, Labadie C, Wahnert M, Leuze C, Streicher M et al (2014) Myelin and iron concentration in the human brain: a quantitative study of MRI contrast. NeuroImage. Google Scholar
  52. Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DGM, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. NeuroImage. Google Scholar
  53. Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4(1):37–48. CrossRefGoogle Scholar
  54. Tournier J-D, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 35(4):1459–1472. CrossRefGoogle Scholar
  55. Tournier J-D, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions | request PDF. In: Proc. Intl. Soc. Mag. Reson. Med, 1670.
  56. Tremblay P, Dick AS (2016) Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain Lang 162:60–71. CrossRefGoogle Scholar
  57. Van Essen DC, Smith SM, Barch DM, Behrens TEJ, Yacoub E, Ugurbil K, WU-Minn HCP Consortium (2013) The WU-Minn Human Connectome Project: an overview. NeuroImage 80:62–79. CrossRefGoogle Scholar
  58. Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, Houde O, Mazoyer B, Tzourio-Mazoyer N (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. NeuroImage 30(4):1414–1432. CrossRefGoogle Scholar
  59. Vu AT, Auerbach E, Lenglet C, Moeller S, Sotiropoulos SN, Jbabdi S, Andersson J, Yacoub E, Ugurbil K (2015) High resolution whole brain diffusion imaging at 7T for the Human Connectome Project. NeuroImage 122(November):318–331. CrossRefGoogle Scholar
  60. Waehnert MD, Dinse J, Schäfer A, Geyer S, Bazin P-L, Turner R, Tardif CL (2016) A subject-specific framework for in vivo myeloarchitectonic analysis using high resolution quantitative MRI. NeuroImage 125:94–107. CrossRefGoogle Scholar
  61. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K et al (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage 36(3):630–644. CrossRefGoogle Scholar
  62. Warren JD, Scott SK, Price CJ, Griffiths TD (2006) Human brain mechanisms for the early analysis of voices. NeuroImage 31(3):1389–1397. CrossRefGoogle Scholar
  63. Weber K, Christiansen MH, Petersson KM, Indefrey P, Hagoort P (2016) FMRI syntactic and lexical repetition effects reveal the initial stages of learning a new language. J Neurosci 36(26):6872–6880. CrossRefGoogle Scholar
  64. Wernicke C (1874) Der aphasische Symptomencomplex: eine psychologische Studie auf anatomischer Basis. Breslau, Cohn and Weigert, WroclawGoogle Scholar
  65. Wilkinson M (2013) Testing the null hypothesis: the forgotten legacy of Karl Popper? J Sports Sci 31(9):919–920. CrossRefGoogle Scholar
  66. Yeatman JD, Dougherty RF, Myall NJ, Wandell BA, Feldman HM (2012) Tract profiles of white matter properties: automating fiber-tract quantification. PLoS One. Google Scholar
  67. Yeatman JD, Wandell BA, Mezer AA (2014) Lifespan maturation and degeneration of human brain white matter. Nat Commun. Google Scholar
  68. Yeo BT, Thomas FM, Krienen JS, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL et al (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106(3):1125–1165. CrossRefGoogle Scholar
  69. Zilles K, Amunts K (2018) Cytoarchitectonic and receptorarchitectonic organization in Broca’s region and surrounding cortex. Curr Opin Behav Sci 21:93–105. CrossRefGoogle Scholar
  70. Zilles K, Bacha-Trams M, Palomero-Gallagher N, Amunts K, Friederici AD (2015) Common molecular basis of the sentence comprehension network revealed by neurotransmitter receptor fingerprints. Cortex 63(February):79–89. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The Edmond and Lily Safra Center for Brain SciencesThe Hebrew University of JerusalemJerusalemIsrael
  2. 2.The Edmond and Lily Safra Center for Brain Sciences, Goodman Building, Room 2202The Hebrew University of Jerusalem, The Edmond J. Safra Campus at Givat RamJerusalemIsrael

Personalised recommendations