Abstract
This study investigates the structure–function relationships between the anatomy of Heschl’s gyri (HG) and speech hemispheric lateralization in 281 healthy volunteers (135 left-handers). Hemispheric lateralization indices (HFLIs) were calculated with Wilke’s method from the activations obtained via functional magnetic resonance imaging while listening to lists of words (LIST). The mean HFLI during LIST was rightward asymmetrical, and left-handers displayed a trend toward decreased rightward asymmetry. The correlations between LIST BOLD contrast maps and individual HFLIs demonstrated that among the cortical areas showing significant asymmetry during LIST, only phonological regions explained HFLI variability. Significant positive correlations were present among the left HG, supramarginal gyri, and the anterior insula. Significant negative correlations occurred in the mid-part of the right superior temporal sulcus. Left HG had the largest functional activity during LIST and explained 10 % of the HFLI variance. There was a strong anatomo-functional link in the HG: duplication was associated with a decrease in both the surface area of the anterior HG and HG functional activity. Participants with a single left HG exhibited leftward anatomical and functional asymmetry of HG, but participants with a left duplication lost either anatomical and/or functional leftward asymmetries. Finally, manual preference was related to HG anatomy, but not to HG functional asymmetries measured during LIST. The anatomical characteristics of left-handers (lower occurrence of right HG duplication and a smaller surface area of the right first HG) thus appeared to be unrelated to variations in speech lateralization with handedness.
Similar content being viewed by others
References
Abdul-Kareem IA, Sluming V (2008) Heschl gyrus and its included primary auditory cortex: structural MRI studies in healthy and diseased subjects. J Magn Reson Imaging 28:287–299
Beaucousin V, Lacheret A, Turbelin MR, Morel M, Mazoyer B, Tzourio-Mazoyer N (2007) FMRI study of emotional speech comprehension. Cereb Cortex 17:339–352
Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B (2000) Voice-selective areas in human auditory cortex. Nature 403:309–312
Binder JR (2011) Functional MRI is a valid noninvasive alternative to Wada testing. Epilepsy Behav 20:214–222. doi:10.1016/j.yebeh.2010.08.004
Boemio A, Fromm S, Braun A, Poeppel D (2005) Hierarchical and asymmetric temporal sensitivity in human auditory cortices. Nat Neurosci 8:389–395. doi:10.1038/nn1409
Clarke S, Rivier F (1998) Compartments within human primary auditory cortex: evidence from cytochrome oxidase and acetylcholinesterase staining. Eur J Neurosci 10:741–745
Corbetta M, Shulman GL (2011) Spatial neglect and attention networks. Annu Rev Neurosci 34:569–599. doi:10.1146/annurev-neuro-061010-113731
Diallo B, Dolidon F, Travere J-, Mazoyer B (1998) VoxeLine: a software for 3D real-time visualization of biomedical images. Comput Med Imaging Graph 22:275–289
Friederici AD, Brauer J, Lohmann G (2011) Maturation of the language network: from inter- to intrahemispheric connectivities. PLoS One 6:e20726. doi:10.1371/journal.pone.0020726
Glasser MF, Rilling JK (2008) DTI tractography of the human brain’s language pathways. Cereb Cortex 18:2471–2482. doi:10.1093/cercor/bhn011
Golestani N, Molko N, Dehaene S, LeBihan D, Pallier C (2007) Brain structure predicts the learning of foreign speech sounds. Cereb Cortex 17:575–582. doi:10.1093/cercor/bhk001
Golestani N, Price CJ, Scott SK (2011) Born with an ear for dialects? Structural plasticity in the expert phonetician brain. J Neurosci 31:4213–4220. doi:10.1523/JNeurosci.3891-10
Hardyck C, Petrinovich LF (1977) Left-handedness. Psychol Bull 84:385–404
Hecaen H, Sauguet J (1971) Cerebral dominance in left-handed subjects. Cortex 7:19–48
Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8:393–402. doi:10.1038/nrn2113
Hill J, Dierker D, Neil J, Inder T, Knutsen A, Harwell J, Coalson T, Van Essen D (2010) A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants. J Neurosci 30:2268–2276. doi:10.1523/JNeurosci.4682-09
Hund-Georgiadis M, Lex U, von Cramon DY (2001) Language dominance assessment by means of FMRI: contributions from task design, performance, and stimulus modality. J Magn Reson Imaging 13:668–675
Hund-Georgiadis M, Lex U, Friederici AD, von Cramon DY (2002) Non-invasive regime for language lateralization in right- and left-handers by means of functional MRI and dichotic listening. Exp Brain Res 145:166–176
Ide A, Dolezal C, Fernández M, Labbé E, Mandujano R, Montes S, Segura P, Verschae G, Yarmuch P, Aboitiz F (1999) Hemispheric differences in variability of fissural patterns in parasylvian and cingulate regions of human brains. J Comp Neurol 410:235–242
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
Josse G, Hervé PY, Crivello F, Mazoyer B, Tzourio-Mazoyer N (2006) Hemispheric specialization for language: brain volume matters. Brain Res 1068:184–193. doi:10.1016/j.brainres.2005.11.037
Knecht S, Dräger B, Deppe M, Bobe L, Lohmann H, Flöel A, Ringelstein EB, Henningsen H (2000) Handedness and hemispheric language dominance in healthy humans. Brain 123:2512–2518
Kulynych JJ, Vladar K, Jones DW, Weinberger DR (1993) Three-dimensional surface rendering in MRI morphometry: a study of the planum temporale. J Comput Assist Tomogr 17:529–535
Leonard CM, Puranik C, Kuldau JM, Lombardino LJ (1998) Normal variation in the frequency and location of human auditory cortex landmarks. Heschl’s gyrus: where is it? Cereb Cortex 8:397–406
Leonard CM, Eckert MA, Lombardino LJ, Oakland T, Kranzler J, Mohr CM, King WM, Freeman A (2001) Anatomical risk factors for phonological dyslexia. Cereb Cortex 11:148–157
Li G, Nie J, Wang L, Shi F, Lyall AE, Lin W, Gilmore JH, and Shen D (2013) Mapping Longitudinal Hemispheric Structural Asymmetries of the Human Cerebral Cortex From Birth to 2 Years of Age. Cereb Cortex. doi:10.1093/cercor/bhs413
Marie D, Jobard G, Crivello F, Perchey G, Petit L, Mellet E, Joliot M, Zago L, Mazoyer B, Tzourio-Mazoyer N (2013) Descriptive anatomy of Heschl’s gyri in 430 healthy volunteers, including 198 left-handers. Brain Struct Funct
Mateer CA, Rapport RL, Kettrick C (1984) Cerebral organization of oral and signed language responses: case study evidence from amytal and cortical stimulation studies. Brain Lang 21:123–135
Morosan P, Rademacher J, Schleicher A, Amunts K, Schormann T, Zilles K (2001) Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 13:684–701
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Penhune VB, Zatorre RJ, MacDonald JD, Evans AC (1996) Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex 6:661–672
Perani D, Saccuman MC, Scifo P, Anwander A, Awander A, Spada D, Baldoli C, Poloniato A, Lohmann G, Friederici AD (2011) Neural language networks at birth. Proc Natl Acad Sci USA 108:16056–16061. doi:10.1073/pnas.1102991108
Petit L, Zago L, Vigneau M, Andersson F, Crivello F, Mazoyer B, Mellet E, Tzourio-Mazoyer N (2009) Functional asymmetries revealed in visually guided saccades: an FMRI study. J Neurophysiol 102:2994. doi:10.1093/cercor/bhp086
Pujol J, Deus J, Losilla JM, Capdevela A (1999) Cerebral lateralization of language in normal left-handed people studied by functional MRI. Neurology 52:1038–1043
Rademacher J, Caviness VS, Steinmetz H, Galaburda AM (1993) Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. Cereb Cortex 3:313–329
Rademacher J, Morosan P, Schormann T, Schleicher A, Werner C, Freund HJ, Zilles K (2001) Probabilistic mapping and volume measurement of human primary auditory cortex. Neuroimage 13:669–683
Razafimandimby A, Tzourio-Mazoyer N, Mazoyer B, Maiza O, Dollfus S (2011) Language lateralization in left-handed patients with schizophrenia. Neuropsychologia 49:313–319
Ressel V, Pallier C, Ventura-Campos N, Díaz B, Roessler A, Avila C, and Sebastián-Gallés N (2012) An effect of bilingualism on the auditory cortex. J Neurosci 32:16597–16601. doi:10.1523/JNeurosci.1996-12.2012
Riecker A, Wildgruber D, Dogil G, Grodd W, Ackermann H (2002) Hemispheric lateralization effects of rhythm implementation during syllable repetitions: an FMRI study. Neuroimage 16:169–176
Rivier F, Clarke S (1997) Cytochrome oxidase, acetylcholinesterase, and NADPH-diaphorase staining in human supratemporal and insular cortex: evidence for multiple auditory areas. Neuroimage 6:288–304
Rosen S, Wise RJ, Chadha S, Conway EJ, Scott SK (2011) Hemispheric asymmetries in speech perception: sense, nonsense and modulations. PLoS One 6:e24672. doi:10.1371/journal.pone.0024672
Schneider P, Sluming V, Roberts N, Scherg M, Goebel R, Specht HJ, Dosch HG, Bleeck S, Stippich C, Rupp A (2005) Structural and functional asymmetry of lateral Heschl’s gyrus reflects pitch perception preference. Nat Neurosci 8:1241–1247. doi:10.1038/nn1530
Seghier ML, Kherif F, Josse G, Price CJ (2011) Regional and hemispheric determinants of language laterality: Implications for preoperative FMRI. Hum Brain Mapp 32:1602–1614. doi:10.1002/hbm
Smith KM, Mecoli MD, Altaye M, Komlos M, Maitra R, Eaton KP, Egelhoff JC, Holland SK (2011) Morphometric differences in the Heschl’s gyrus of hearing impaired and normal hearing infants. Cereb Cortex 21:991–998. doi:10.1093/cercor/bhq164
Springer JA, Binder JR, Hammeke TA, Swanson SJ, Frost JA, Bellgowan PS, Brewer CC, Perry HM, Morris GL, Mueller WM (1999) Language dominance in neurologically normal and epilepsy subjects—a functional MRI study. Brain 122:2033–2045
Szaflarski JP, Binder JR, Possing ET, McKiernan KA, Ward BD, Hammeke TA (2002) Language lateralization in left-handed and ambidextrous people: FMRI data. Neurology 59:238–244
Szaflarski JP, Rajagopal A, Altaye M, Byars AW, Jacola L, Schmithorst VJ, Schapiro MB, Plante E, Holland SK (2011) Left-handedness and language lateralization in children. Brain Res 1433:85–97. doi:10.1016/j.brainres.2011.11.026
Takai O, Brown S, Liotti M (2010) Representation of the speech effectors in the human motor cortex: somatotopy or overlap? Brain Lang 113:39–44. doi:10.1016/j.bandl.2010.01.008
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. doi:10.1006/nimg.1998.0343
Tzourio N, Nkanga-Ngila B, Mazoyer B (1998b) Left planum temporale surface correlates with functional dominance during story listening. Neuroreport 9:829–833
Tzourio-Mazoyer N, Josse G, Crivello F, Mazoyer B (2004) Interindividual variability in the hemispheric organization for speech. Neuroimage 21:422–435
Tzourio-Mazoyer N, Simon G, Crivello F, Jobard G, Zago L, Perchey G, Hervé PY, Joliot M, Petit L, Mellet E, Mazoyer B (2010) Effect of familial sinistrality on planum temporale surface and brain tissue asymmetries. Cereb Cortex 20:1476–1485. doi:10.1093/cercor/bhp209
Vigneau M, Beaucousin V, Hervé PY, Duffau H, Crivello F, Houdé O, Mazoyer B, Tzourio-Mazoyer N (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30:1414–1432. doi:10.1016/j.neuroimage.2005.11.002
Vingerhoets G, Alderweireldt AS, Vandemaele P, Cai Q, Van der Haegen L, Brysbaert M, Achten E (2011) Praxis and language are linked: evidence from co-lateralization in individuals with atypical language dominance. Cortex 49:172–183. doi:10.1016/j.cortex.2011.11.003
Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralisation of cerebral speech dominance. J Neurosurg 17:226–282
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 29:61–69. doi:10.1523/JNeurosci.3489-08
Westerhausen R, Kompus K, and Hugdahl K (2013) Mapping hemispheric symmetries, relative asymmetries, and absolute asymmetries underlying the auditory laterality effect. Neuroimage 84:962–970. doi:10.1016/j.neuroimage.2013.09.074
Wildgruber D, Riecker A, Hertrich I, Erb M, Grodd W, Ethofer T, Ackermann H (2005) Identification of emotional intonation evaluated by FMRI. Neuroimage 24:1233–1241. doi:10.1016/j.neuroimage.2004.10.034
Wilke M, Lidzba K (2007) LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods 163:128–136
Wilke M, Schmithorst VJ (2006) A combined bootstrap/histogram analysis approach for computing a lateralization index from neuroimaging data. Neuroimage 33:522–530. doi:10.1016/j.neuroimage.2006.07.010
Wong PC, Warrier CM, Penhune VB, Roy AK, Sadehh A, Parrish TB, Zatorre RJ (2008) Volume of left Heschl’s Gyrus and linguistic pitch learning. Cereb Cortex 18:828–836. doi:10.1093/cercor/bhm115
Zago L, Tzourio-Mazoyer N (2002) Distinguishing visuospatial working memory and mental complex calculation areas within the parietal lobes. Neurosci Lett 331:45–49
Zatorre RJ, Belin P (2001) Spectral and temporal processing in human auditory cortex. Cerebral Cortex 11:946–953
Zatorre RJ, Gandour JT (2008) Neural specializations for speech and pitch: moving beyond the dichotomies. Philos Trans R Soc Lond B Biol Sci 363:1087–1104. doi:10.1098/rstb.2007.2161
Zatorre RJ, Bouffard M, Ahad P, Belin P (2002) Where is ‘where’ in the human auditory cortex? Nat Neurosci 5:905–909
Acknowledgments
The authors are deeply indebted to Mathieu Vigneau and Nicolas Delcroix for their help in data acquisition and pre-processing and to the Aquitaine Regional Council for its funding of Damien Marie PhD. They are also very grateful to two anonymous reviewers whose fruitful comments allowed us to provide a more elaborated version of the manuscript and to Isabelle Hesling for her thoughtful comments on the revised version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tzourio-Mazoyer, N., Marie, D., Zago, L. et al. Heschl’s gyrification pattern is related to speech-listening hemispheric lateralization: FMRI investigation in 281 healthy volunteers. Brain Struct Funct 220, 1585–1599 (2015). https://doi.org/10.1007/s00429-014-0746-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-014-0746-4