Skip to main content
Log in

Is the planum temporale surface area a marker of hemispheric or regional language lateralization?

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

We investigated the association between the left planum temporale (PT) surface area or asymmetry and the hemispheric or regional functional asymmetries during language production and perception tasks in 287 healthy adults (BIL&GIN) who were matched for sex and handedness. The measurements of the PT surface area were performed after manually delineating the region using brain magnetic resonance images (MRI) and considering the Heschl’s gyrus (HG) duplication pattern; the measurements either included (PTtot) or did not include (PTpost) the second gyrus. A region encompassing both the PT and HG (HGPT) was also studied. Regardless of the ROI measured, 80% of the sample had a positive left minus right PT asymmetry. We first tested whether the PTtot, PTpost and HGPT surface areas in the left or right hemispheres or PT asymmetries differed in groups of individuals varying in language lateralization by assessing their hemispheric index during a sentence production minus word list production task. We then investigated the association between these different measures of the PT anatomy and the regional asymmetries measured during the task. Regardless of the anatomical definition used, we observed no correlations between the left surface areas or asymmetries and the hemispheric or regional functional asymmetries during the language production task. We then performed a similar analysis using the same sample measuring language functional lateralization during speech listening tasks (i.e., listening to sentences and lists of words). Although the hemispheric lateralization during speech listening was not correlated with the left PTtot, PTpost or HGPT surface areas or the PT asymmetries, significant positive correlations were observed between the asymmetries in these regions and the regional functional asymmetries measured in areas adjacent to the end of the Sylvian fissure while participants listened to the word lists or sentences. The PT asymmetry thus appears to be associated with the local functional asymmetries in auditory areas but is not a marker of inter-individual variability in language dominance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altarelli I, Leroy F, Monzalvo K, Fluss J, Billard C, Dehaene-Lambertz G, Galaburda AM, Ramus F (2014) Planum temporale asymmetry in developmental dyslexia: revisiting an old question. Hum Brain Mapp 35:5717–5735

    Article  PubMed  Google Scholar 

  • Andoh J, Matsushita R, Zatorre RJ (2015) Asymmetric interhemispheric transfer in the auditory network: evidence from TMS, resting-State fMRI, and diffusion imaging. J Neurosci 35:14602–14611

    Article  CAS  PubMed  Google Scholar 

  • Barrick TR, Mackay CE, Prima S, Maes F, Vandermeulen D, Crow TJ, Roberts N (2005) Automatic analysis of cerebral asymmetry: an exploratory study of the relationship between brain torque and planum temporale asymmetry. Neuroimage 24:678–691

    Article  PubMed  Google Scholar 

  • Bishop DVM (2013) Cerebral asymmetry and language development: cause, correlate, or consequence? Science 340:1230531

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark GM, Crow TJ, Barrick TR, Collinson SL, James AC, Roberts N, Mackay CE (2010) Asymmetry loss is local rather than global in adolescent onset schizophrenia. Schizophr Res 120:84–86

    Article  PubMed  Google Scholar 

  • Dorsaint-Pierre R, Penhune VB, Watkins KE, Neelin P, Lerch JP, Bouffard M, Zatorre RJ (2006) Asymmetries of the planum temporale and Heschl’s gyrus: relationship to language lateralization. Brain 129:1164–1176

    Article  PubMed  Google Scholar 

  • Dym RJ, Burns J, Freeman K, Lipton ML (2011) Is functional MR imaging assessment of hemispheric language dominance as good as the Wada test?: a meta-analysis. Radiology 261:446–455

    Article  PubMed  Google Scholar 

  • Floris DL, Lai MC, Auer T, Lombardo MV, Ecker C, Chakrabarti B, Wheelwright SJ, Bullmore ET, Murphy DG, Baron-Cohen S, Suckling J (2016) Atypically rightward cerebral asymmetry in male adults with autism stratifies individuals with and without language delay. Hum Brain Mapp 37:230–253

    Article  PubMed  Google Scholar 

  • Foundas AL, Leonard CM, Gilmore R, Fennell E, Heilman KM (1994) Planum temporale asymmetry and language dominance. Neuropsychologia 32:1225–1231

    Article  CAS  PubMed  Google Scholar 

  • Foundas AL, Leonard CM, Heilman KM (1995) Morphological asymmetries and handedness. The pars triangularis and planum temporale. Arch Neurol 52:501–508

    Article  CAS  PubMed  Google Scholar 

  • Galaburda AM, Sanides F, Geschwind N (1978) Human brain. Cytoarchitectonic left-right asymmetries in the temporal speech region. Arch Neurol 35:812–817

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Habib M, Gayraud D, Oliva A, Regis J, Salamon G, Khalil R (1991) Effects of handedness and sex on the morphology of the corpus callosum: a study with brain magnetic resonance imaging. Brain Cogn 16:41–61

    Article  CAS  PubMed  Google Scholar 

  • Hasan A, Kremer L, Gruber O, Schneider-Axmann T, Guse B, Reith W, Falkai P, Wobrock T (2011) Planum temporale asymmetry to the right hemisphere in first-episode schizophrenia. Psychiatry Res 193:56–59

    Article  PubMed  Google Scholar 

  • Hécaen H, De Agostini M, Monzon-Montes A (1981) Cerebral organization in left-handers. Brain Lang 12:261–284

    Article  PubMed  Google Scholar 

  • Jäncke L, Steinmetz H (1993) Auditory lateralization and planum temporale asymmetry. Neuroreport 5:169–172

    Article  PubMed  Google Scholar 

  • Joliot M, Jobard G, Naveau M, Delcroix N, Petit L, Zago L, Crivello F, Mellet E, Mazoyer B, Tzourio-Mazoyer N (2015) AICHA: an atlas of intrinsic connectivity of homotopic areas. J Neurosci Methods 254:46–59

    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 

  • Josse G, Hervé PY, Crivello F, Mazoyer B, Tzourio-Mazoyer N (2006) Hemispheric specialization for language: brain volume matters. Brain Res 1068:184–193

    Article  CAS  PubMed  Google Scholar 

  • Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Onitsuka T, Spencer MH, Yurgelun-Todd DA, Kikinis R, Jolesz FA, McCarley RW (2003) Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 60:766–775

    Article  PubMed  PubMed Central  Google Scholar 

  • Keller SS, Roberts N, García-Fiñana M, Mohammadi S, Ringelstein EB, Knecht S, Deppe M (2011) Can the language-dominant hemisphere be predicted by brain anatomy? J Cogn Neurosci 23:2013–2029

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Leonard CM, Lombardino LJ, Walsh K, Eckert MA, Mockler JL, Rowe LA, Williams S, DeBose CB (2002) Anatomical risk factors that distinguish dyslexia from SLI predict reading skill in normal children. J Commun Disord 35:501–531

    Article  PubMed  Google Scholar 

  • 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 220:729–743

    Article  PubMed  PubMed Central  Google Scholar 

  • Mazoyer B, Zago L, Jobard G, Crivello F, Joliot M, Perchey G, Mellet E, Petit L, Tzourio-Mazoyer N (2014) Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS One 9:e101165

    Article  PubMed  PubMed Central  Google Scholar 

  • Mazoyer B, Mellet E, Perchey G, Zago L, Crivello F, Jobard G, Delcroix N, Vigneau M, Leroux G, Petit L, Joliot M, Tzourio-Mazoyer N (2016) BIL&GIN: a neuroimaging, cognitive, behavioral, and genetic database for the study of human brain lateralization. Neuroimage 124:1225–1231

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Satz P (1979) A test of some models of hemispheric speech organization in the left- and right-handed. Science 203:1131–1133

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  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 Rev 29:26–49

    Article  CAS  PubMed  Google Scholar 

  • Somers M, Aukes MF, Ophoff RA, Boks MP, Fleer W, de Visser KL, Kahn RS, Sommer IE (2015) On the relationship between degree of hand-preference and degree of language lateralization. Brain Lang 144:10–15

    Article  PubMed  Google Scholar 

  • Steinmetz H, Rademacher J, Huang Y, Hefter H, Zilles K, Thron A, Freund H- (1989) Cerebral asymmetry: MR planimetry of the human planum temporale. J Comput Assist Tomogr 13:996–1005

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Teszner D, Tzavaras A, Gruner J, Hecaen H (1972) L’asymetrie droite-gauche du planum temporale; a propos de l’etude anatomique de 100 cerveaux. Revue neurologique 126:444–449

    CAS  PubMed  Google Scholar 

  • Tzourio-Mazoyer N, Mazoyer B (2017) Variations of planum temporale asymmetries with Heschl’s Gyri duplications and association with cognitive abilities: MRI investigation of 428 healthy volunteers. Brain Struct Funct 222:2711–2726

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Tzourio-Mazoyer N, Marie D, Zago L, Jobard G, Perchey G, Leroux G, Mellet E, Joliot M, Crivello F, Petit L, Mazoyer B (2014) Heschl’s gyrification pattern is related to speech-listening hemispheric lateralization: fMRI investigation in 281 healthy volunteers. Brain Struct Funct 220:1585–1599

    Article  PubMed  Google Scholar 

  • Tzourio-Mazoyer N, Joliot M, Marie D, Mazoyer B (2015) Variation in homotopic areas’ activity and inter-hemispheric intrinsic connectivity with type of language lateralization: an fMRI study of covert sentence generation in 297 healthy volunteers. Brain Struct Funct 221:2735–2753

    Article  PubMed  Google Scholar 

  • van der Knaap LJ, van der Ham IJ (2011) How does the corpus callosum mediate interhemispheric transfer? A review. Behav Brain Res 223:211–221

    Article  PubMed  Google Scholar 

  • Wilke M, Lidzba K (2007) LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods 163:128–136

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the FLAG-ERA Human Brain Project 2015 (ANR-15-HBPR-0001-03-MULTI-LATERAL) to BM, NTM, and FC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nathalie Tzourio-Mazoyer.

Ethics declarations

Ethics statement

The study has been approved by the Basse-Normandie research ethics committee and have been performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Informed consent

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

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tzourio-Mazoyer, N., Crivello, F. & Mazoyer, B. Is the planum temporale surface area a marker of hemispheric or regional language lateralization?. Brain Struct Funct 223, 1217–1228 (2018). https://doi.org/10.1007/s00429-017-1551-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-017-1551-7

Keywords

Navigation