Abstract
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.
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References
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):319–341
Amunts K, Schleicher A, Ditterich A, Zilles K (2003) Broca’s region: cytoarchitectonic asymmetry and developmental changes. J Comp Neurol 465(1):72–89. https://doi.org/10.1002/cne.10829
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. https://doi.org/10.1016/j.neuroimage.2010.09.025
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. https://doi.org/10.1002/hbm.24626
Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15(7–8):435–455. https://doi.org/10.1002/nbm.782
Bodin C, Takerkart S, Belin P, Coulon O (2018) Anatomo-functional correspondence in the superior temporal sulcus. Brain Struct Funct 223(1):221–232. https://doi.org/10.1007/s00429-017-1483-2
Broca P (1865) Sur Le Siège de La Faculté Du Langage Articulé. Bulletins de La Société d’anthropologie de Paris 1(6):377–393. https://doi.org/10.3406/bmsap.1865.9495
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. https://doi.org/10.1016/j.neuroimage.2017.11.066
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. https://doi.org/10.1073/pnas.0702116104
Cercignani M, D NG, Tofts Paul (eds) (2018) Quantitative MRI of the brain: principles of physical measurement, 2nd edn. CRC Press, London
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. https://doi.org/10.1002/mrm.21669
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. https://doi.org/10.1093/cercor/bhx244
Daducci A, Dal Palú A, Descoteaux M, Thiran J-P (2016) Microstructure informed tractography: pitfalls and open challenges. Front Neurosci. https://doi.org/10.3389/fnins.2016.00247
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):3809–3815
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. https://doi.org/10.1016/j.neuroimage.2006.01.021
DeWitt I, Rauschecker JP (2013) Wernicke’s area revisited: parallel streams and word processing. Brain Lang 127(2):181–191. https://doi.org/10.1016/j.bandl.2013.09.014
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):3403
Geschwind N (1970) The organization of language and the brain. Science 170(3961):940–944
Geschwind N, Levitsky W (1968) Human brain: left–right asymmetries in temporal speech region. Science 161(3837):186–187. https://doi.org/10.1126/science.161.3837.186
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. https://doi.org/10.1016/j.neuroimage.2013.04.127
Hagoort P (2014) Nodes and networks in the neural architecture for language: Broca’s region and beyond. Curr Opin Neurobiol 28:136–141. https://doi.org/10.1016/j.conb.2014.07.013
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. https://doi.org/10.1016/B978-0-12-407794-2.00025-0
Hilgetag CC, Barbas H (2006) Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2(3):e22. https://doi.org/10.1371/journal.pcbi.0020022
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. https://doi.org/10.1016/S0093-934X(02)00531-X
Hutsler JJ, Galuske RAW (2003) Hemispheric asymmetries in cerebral cortical networks. Trends Neurosci 26(8):429–435. https://doi.org/10.1016/S0166-2236(03)00198-X
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. https://doi.org/10.1016/j.neuroimage.2012.06.081
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. https://doi.org/10.1016/j.bandl.2008.11.005
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. https://doi.org/10.1073/pnas.1718418115
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. https://doi.org/10.1016/j.neuroimage.2018.03.046
Lebois A (2014) Brain microstructure mapping using quantitative and diffusion MRI. PhD thesis, Université Paris Sud-Paris XI. https://tel.archives-ouvertes.fr/tel-01063198/document
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. https://doi.org/10.1073/pnas.1412389112
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. https://doi.org/10.1073/pnas.1301696110
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. https://doi.org/10.1073/pnas.1608282113
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. https://doi.org/10.1016/j.neuropsychologia.2012.01.010
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. https://doi.org/10.1016/j.neuroimage.2012.05.052
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):1667–1672
Mezer A, Rokem A, Berman S, Hastie T, Wandell BA (2016) Evaluating quantitative proton-density-mapping methods. Hum Brain Mapp 37(10):3623–3635. https://doi.org/10.1002/hbm.23264
Nucifora PGP, Verma R, Melhem ER, Gur RE, Gur RC (2005) Leftward asymmetry in relative fiber density of the arcuate fasciculus. NeuroReport 16(8):791–794
Pestilli F, Yeatman JD, Rokem A, Kay KN, Wandell BA (2014) Evaluation and statistical inference for living connectomes. Nat Methods 11(10):1058–1063. https://doi.org/10.1038/nmeth.3098
Poeppel D, Hickok G (2004) Towards a new functional anatomy of language. Cognition 92(1–2):1–12. https://doi.org/10.1016/j.cognition.2003.11.001
Popper K (1962) The logic of scientific discovery, revised edition. Hutchinson, Paris
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. https://doi.org/10.1038/s41598-017-17314-0
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. https://doi.org/10.1002/mrm.10308
Rilling JK (2014) Comparative primate neurobiology and the evolution of brain language systems. Curr Opin Neurobiol 28:10–14. https://doi.org/10.1016/j.conb.2014.04.002
Rilling JK, Glasser MF, Jbabdi S, Andersson J, Preuss TM (2012) Continuity, divergence, and the evolution of brain language pathways. Front Evol Neurosci. https://doi.org/10.3389/fnevo.2011.00011
Rogalsky C, Hickok G (2010) The role of Broca’s area in sentence comprehension. J Cogn Neurosci 23(7):1664–1680. https://doi.org/10.1162/jocn.2010.21530
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. https://doi.org/10.1016/j.cortex.2017.09.002
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. https://doi.org/10.1093/cercor/bhp138
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. https://doi.org/10.1002/mrm.26653
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. https://doi.org/10.1016/j.neuroimage.2012.06.005
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. https://doi.org/10.1016/j.neuroimage.2014.02.026
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. https://doi.org/10.1016/j.neuroimage.2010.07.055
Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4(1):37–48. https://doi.org/10.1038/nrn1009
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. https://doi.org/10.1016/j.neuroimage.2007.02.016
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. https://cds.ismrm.org/protected/10MProceedings/files/1670_4298.pdf
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
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. https://doi.org/10.1016/j.neuroimage.2013.05.041
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. https://doi.org/10.1016/j.neuroimage.2005.11.002
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. https://doi.org/10.1016/j.neuroimage.2015.08.004
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. https://doi.org/10.1016/j.neuroimage.2015.10.001
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. https://doi.org/10.1016/j.neuroimage.2007.02.049
Warren JD, Scott SK, Price CJ, Griffiths TD (2006) Human brain mechanisms for the early analysis of voices. NeuroImage 31(3):1389–1397. https://doi.org/10.1016/j.neuroimage.2006.01.034
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. https://doi.org/10.1523/JNEUROSCI.3180-15.2016
Wernicke C (1874) Der aphasische Symptomencomplex: eine psychologische Studie auf anatomischer Basis. Breslau, Cohn and Weigert, Wroclaw
Wilkinson M (2013) Testing the null hypothesis: the forgotten legacy of Karl Popper? J Sports Sci 31(9):919–920. https://doi.org/10.1080/02640414.2012.753636
Yeatman JD, Dougherty RF, Myall NJ, Wandell BA, Feldman HM (2012) Tract profiles of white matter properties: automating fiber-tract quantification. PLoS One. https://doi.org/10.1371/journal.pone.0049790
Yeatman JD, Wandell BA, Mezer AA (2014) Lifespan maturation and degeneration of human brain white matter. Nat Commun. https://doi.org/10.1038/ncomms5932
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. https://doi.org/10.1152/jn.00338.2011
Zilles K, Amunts K (2018) Cytoarchitectonic and receptorarchitectonic organization in Broca’s region and surrounding cortex. Curr Opin Behav Sci 21:93–105. https://doi.org/10.1016/j.cobeha.2018.02.011
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. https://doi.org/10.1016/j.cortex.2014.07.007
Acknowledgements
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.
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This work was supported by the United States–Israel Binational Science Foundation (BCS1551330 to AAM); the Israel Science Foundation (0399306 to AAM).
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Bain, J.S., Filo, S. & Mezer, A.A. The robust and independent nature of structural STS asymmetries. Brain Struct Funct 224, 3171–3182 (2019). https://doi.org/10.1007/s00429-019-01952-3
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DOI: https://doi.org/10.1007/s00429-019-01952-3