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

Abstract

We investigated the regional correlates of differences in hemispheric lateralization in 297 healthy volunteers [including 153 left-handers (LH)] previously classified into three types of language lateralization according to their hemispheric functional lateralization index measured with fMRI during covert sentence production versus word list production (PRODSENT-LIST): 250 leftward asymmetrical Typicals, 10 rightward asymmetrical Strong-atypicals (only LH), and 37 Ambilaterals with weak lateralization. Using a functionally driven homotopic atlas (AICHA), we compared patterns of regional asymmetry during PRODSENT-LIST in these three groups. Among the 192 homotopic regions of interest (hROIs) of the AICHA atlas, 58 exhibited a significant effect of the type of lateralization on their BOLD signal variation during PRODSENT-LIST. The analyses of patterns of asymmetry of these 58 hROIs showed that (1) hROIs asymmetries in Strong-atypicals were significantly negatively correlated with those observed in Typicals, which indicates that their regional pattern of rightward asymmetries was comparable to the regional pattern of leftward language asymmetries of Typicals; (2) right- and left-handed Typicals had identical profiles, whereas left-handed Ambilaterals exhibited reduced leftward asymmetry as compared either to right-handed Ambilaterals or to Typicals. Moreover, left-handed Ambilaterals pattern of hROIs asymmetries significantly positively correlated with those of both Typicals and Strong-atypicals. In 291 of the participants, we tested the hypothesis that differences in language lateralization were associated with differences in inter-hemispheric connectivity during resting state by measuring their regional homotopic inter-hemispheric intrinsic connectivity coefficient (rHIICC) in 36 of the 58 hROIs known to be connected via the corpus callosum. Mean rHIICCs were negatively correlated with task-induced functional asymmetries, suggesting that enhanced inter-hemispheric cooperation at rest translates into increased inter-hemispheric cooperation during language production. In addition, the left-handed Ambilaterals exhibited a significantly larger rHIICC compared with right-handed Ambilaterals and Typicals, confirming a difference in inter-hemispheric organization in this group

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Alexander DC, Hubbard PL, Hall MG, Moore EA, Ptito M, Parker GJ, Dyrby TB (2010) Orientationally invariant indices of axon diameter and density from diffusion MRI. Neuroimage 52:1374–1389

    Article  PubMed  Google Scholar 

  2. Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL (2007) Disruption of large-scale brain systems in advanced aging. Neuron 56:924–935

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Annett M (1998) Handedness and cerebral dominance: the right shift theory. J Neuropsychiatry Clin Neurosci 10:459–469

    CAS  Article  PubMed  Google Scholar 

  4. Berl MM, Zimmaro LA, Khan OI, Dustin I, Ritzl E, Duke ES, Sepeta LN, Sato S, Theodore WH, Gaillard WD (2013) Characterization of atypical language activation patterns in focal epilepsy. Ann Neurol 75:33–42

    Article  Google Scholar 

  5. Binder JR (2011) Functional MRI is a valid noninvasive alternative to Wada testing. Epilepsy Behav 20:214–222

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bishop DV, Holt G, Whitehouse AJ, Groen M (2014) No population bias to left-hemisphere language in 4-year-olds with language impairment. Peer J 2:e507

    Article  PubMed  PubMed Central  Google Scholar 

  7. Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S, Dogonowski AM, Ernst M, Fair D, Hampson M, Hoptman MJ, Hyde JS, Kiviniemi VJ, Kötter R, Li SJ, Lin CP, Lowe MJ, Mackay C, Madden DJ, Madsen KH, Margulies DS, Mayberg HS, McMahon K, Monk CS, Mostofsky SH, Nagel BJ, Pekar JJ, Peltier SJ, Petersen SE, Riedl V, Rombouts SA, Rypma B, Schlaggar BL, Schmidt S, Seidler RD, Siegle GJ, Sorg C, Teng GJ, Veijola J, Villringer A, Walter M, Wang L, Weng XC, Whitfield-Gabrieli S, Williamson P, Windischberger C, Zang YF, Zhang HY, Castellanos FX, Milham MP (2010) Toward discovery science of human brain function. Proc Natl Acad Sci USA 107:4734–4739

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Branch C, Milner B, Rasmussen T (1964) Intracarotid sodium amytal for the lateralization of cerebral speech dominance: observation in 123 patients. J Neurosurg 21:399–405

    CAS  Article  PubMed  Google Scholar 

  9. Chang EF, Wang DD, Perry DW, Barbaro NM, Berger MS (2011) Homotopic organization of essential language sites in right and bilateral cerebral hemispheric dominance. J Neurosurg 114:893–902

    Article  PubMed  Google Scholar 

  10. 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 

  11. Drane DL, Roraback-Carson J, Hebb AO, Hersonskey T, Lucas T, Ojemann GA, Lettich E, Silbergeld DL, Miller JW, Ojemann JG (2012) Cortical stimulation mapping and Wada results demonstrate a normal variant of right hemisphere language organization. Epilepsia 53(10):1790–1798

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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 

  13. Friederici AD, Gierhan SM (2013) The language network. Curr Opin Neurobiol 23:250–254

    CAS  Article  PubMed  Google Scholar 

  14. Gallagher HL, Frith CD (2003) Functional imaging of ‘theory of mind’. Trends Cogn Sci 7:77–83

    Article  PubMed  Google Scholar 

  15. Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? Brain 123:1293–1326

    Article  PubMed  Google Scholar 

  16. Hardyck C, Petrinovich LF (1977) Left-handedness. Psychol Bull 84:385–404

    CAS  Article  PubMed  Google Scholar 

  17. Hecaen H, Sauguet J (1971) Cerebral dominance in left-handed subjects. Cortex 7:19–48

    CAS  Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  19. Hervé P-Y, Zago L, Petit L, Mazoyer B, Tzourio-Mazoyer N (2013) Revisiting human hemispheric specialization with neuroimaging. Trends Cogn Sci 17:69–80

    Article  PubMed  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. Isaacs KL, Barr WB, Nelson PK, Devinsky O (2006) Degree of handedness and cerebral dominance. Neurology 66:1855–1858

    Article  PubMed  Google Scholar 

  22. Joliot M, Naveau M, Herve P-Y, Petit L, Zago L, Crivello F, Jobard G, Mellet E, Tzourio-Mazoyer N, Mazoyer B (2012) Establishing homotopic inter-hemispheric regional correspondences via rest functional connectivity. In: 18th annual meeting of the organization for human brain mapping

  23. 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

    Article  PubMed  Google Scholar 

  24. Liu H, Stufflebeam SM, Sepulcre J, Hedden T, Buckner RL (2009) Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors. Proc Natl Acad Sci USA 106:20499–20503

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Mateer CA, Dodrill CB (1983) Neuropsychological and linguistic correlates of atypical language lateralization: evidence from sodium amytal studies. Hum Neurobiol 2:135–142

    CAS  PubMed  Google Scholar 

  26. 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 

  27. 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 (2015) BIL&GIN: a neuroimaging, cognitive, behavioral, and genetic database for the study of human brain lateralization. Neuroimage. doi:10.1016/j.neuroimage.2015.02.071

    Google Scholar 

  28. Miller JW, Dodrill CB, Born DE, Ojemann GA (2003) Atypical speech is rare in individuals with normal developmental histories. Neurology 60:1042–1044

    CAS  Article  PubMed  Google Scholar 

  29. Miller JW, Jayadev S, Dodrill CB, Ojemann GA (2005) Gender differences in handedness and speech lateralization related to early neurologic insults. Neurology 65:1974–1975

    Article  PubMed  Google Scholar 

  30. Möddel G, Lineweaver T, Schuele SU, Reinholz J, Loddenkemper T (2009) Atypical language lateralization in epilepsy patients. Epilepsia 50:1505–1516

    Article  PubMed  Google Scholar 

  31. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    CAS  Article  PubMed  Google Scholar 

  32. Paulesu E, Frith CD, Frackowiak RSJ (1993) The neural correlates of the verbal component of working memory. Nature 362:342–345

    CAS  Article  PubMed  Google Scholar 

  33. Perani D, Cappa SF, Tettamanti M, Rosa M, Scifo P, Miozzo A, Basso A, Fazio F (2003) A fMRI study of word retrieval in aphasia. Brain Lang 85:357–368

    CAS  Article  PubMed  Google Scholar 

  34. Price CJ (2012) A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 62:816–847

    Article  PubMed  PubMed Central  Google Scholar 

  35. Price CJ, Crinion J (2005) The latest on functional imaging studies of aphasic stroke. Curr Opin Neurol 18:429–434

    Article  PubMed  Google Scholar 

  36. 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

    CAS  Article  PubMed  Google Scholar 

  37. Raja Beharelle A, Dick AS, Josse G, Solodkin A, Huttenlocher PR, Levine SC, Small SL (2010) Left hemisphere regions are critical for language in the face of early left focal brain injury. Brain 133:1707–1716

    Article  PubMed  PubMed Central  Google Scholar 

  38. Rasmussen T, Milner B (1977) The role of early left brain injury in determining lateralization of cerebral speech functions. Ann NY Acad Sci 299:355–369

    CAS  Article  PubMed  Google Scholar 

  39. Rey M, Dellatolas G, Bancaud J, Talairach J (1988) Hemispheric lateralization of motor and speech functions after early brain lesion: study of 73 epileptic patients with intracarotid amytal test. Neuropsychologia 26:167–172

    CAS  Article  PubMed  Google Scholar 

  40. Risse GL, Gates JR, Fangman MC (1997) A reconsideration of bilateral language representation based on the intracarotid amobarbital procedure. Brain Cognition 33:118–132

    CAS  Article  PubMed  Google Scholar 

  41. Rosen HJ, Petersen SE, Linenweber MR, Snyder AZ, White DA, Chapman L, Dromerick AW, Fiez JA, Corbetta M (2000) Neural correlates of recovery from aphasia after damage to left inferior frontal cortex. Neurology 55:1883–1894

    CAS  Article  PubMed  Google Scholar 

  42. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040–13045

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Stark DE, Margulies DS, Shehzad ZE, Reiss P, Kelly AM, Uddin LQ, Gee DG, Roy AK, Banich MT, Castellanos FX, Milham MP (2008) Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations. J Neurosci 28:13754–13764

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Strauss E, Wada J (1983) Lateral preferences and cerebral speech dominance. Cortex 19:165–177

    CAS  Article  PubMed  Google Scholar 

  45. 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 

  46. 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

    CAS  Article  PubMed  Google Scholar 

  47. Vigneau M, Beaucousin V, Hervé PY, Jobard G, Petit L, Crivello F, Mellet E, Zago L, Mazoyer B, Tzourio-Mazoyer N (2011) What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis. Neuroimage 54:577–593

    CAS  Article  PubMed  Google Scholar 

  48. Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralisation of cerebral speech dominance. J Neurosurg 17:226–282

    Article  Google Scholar 

  49. Weiller C, Isensee C, Rijintjes M, Huber W, Müller S, Bier D, Dutschka K, Woods RP, Noth J, Diener HC (1995) Recovery from Wernicke’s aphasia: a positron emission tomographic study. Ann Neurol 37:723–732

    CAS  Article  PubMed  Google Scholar 

  50. Whitehouse AJO, Bishop DVM (2009) Hemispheric division of function is the result of independent probabilistic biases. Neuropsychologia 47:1938–1943

    Article  PubMed  PubMed Central  Google Scholar 

  51. 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 

  52. Willems RM, Clevis K, Hagoort P (2011) Add a picture for suspense: neural correlates of the interaction between language and visual information in the perception of fear. Soc Cogn Affect Neurosci 6:404–416

    Article  PubMed  PubMed Central  Google Scholar 

  53. Woods RP, Dodrill CB, Ojemann GA (1988) Brain injury, handedness, and speech lateralization in a series of amobarbital studies. Ann Neurol 23:510–518

    CAS  Article  PubMed  Google Scholar 

  54. Zatorre RJ (1989) Perceptual asymmetry on the dichotic fused words test and cerebral speech lateralization determined by the carotid sodium amytal test. Neuropsychologia 27:1207–1219

    CAS  Article  PubMed  Google Scholar 

  55. Zuo XN, Kelly C, Di Martino A, Mennes M, Margulies DS, Bangaru S, Grzadzinski R, Evans AC, Zang YF, Castellanos X, Milham MP (2010) Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci 30:15034–15043

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors are deeply grateful to the two anonymous reviewers who completed a very thorough analysis of the article along with thoughtful comments that greatly improved the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nathalie Tzourio-Mazoyer.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tzourio-Mazoyer, N., Joliot, M., Marie, D. et al. 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 (2016). https://doi.org/10.1007/s00429-015-1068-x

Download citation

Keywords

  • fMRI
  • Language
  • Hemispheric specialization
  • Handedness
  • Asymmetries
  • Production
  • Resting state
  • Inter-hemispheric interactions
  • Corpus callosum