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
Similar content being viewed by others
References
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
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
Annett M (1998) Handedness and cerebral dominance: the right shift theory. J Neuropsychiatry Clin Neurosci 10:459–469
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
Binder JR (2011) Functional MRI is a valid noninvasive alternative to Wada testing. Epilepsy Behav 20:214–222
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
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
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
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
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
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
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
Friederici AD, Gierhan SM (2013) The language network. Curr Opin Neurobiol 23:250–254
Gallagher HL, Frith CD (2003) Functional imaging of ‘theory of mind’. Trends Cogn Sci 7:77–83
Gazzaniga MS (2000) Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? Brain 123:1293–1326
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
Hécaen H, De Agostini M, Monzon-Montes A (1981) Cerebral organization in left-handers. Brain Lang 12:261–284
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
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
Isaacs KL, Barr WB, Nelson PK, Devinsky O (2006) Degree of handedness and cerebral dominance. Neurology 66:1855–1858
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
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
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
Mateer CA, Dodrill CB (1983) Neuropsychological and linguistic correlates of atypical language lateralization: evidence from sodium amytal studies. Hum Neurobiol 2:135–142
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
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
Miller JW, Dodrill CB, Born DE, Ojemann GA (2003) Atypical speech is rare in individuals with normal developmental histories. Neurology 60:1042–1044
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
Möddel G, Lineweaver T, Schuele SU, Reinholz J, Loddenkemper T (2009) Atypical language lateralization in epilepsy patients. Epilepsia 50:1505–1516
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Paulesu E, Frith CD, Frackowiak RSJ (1993) The neural correlates of the verbal component of working memory. Nature 362:342–345
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
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
Price CJ, Crinion J (2005) The latest on functional imaging studies of aphasic stroke. Curr Opin Neurol 18:429–434
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
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
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
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
Risse GL, Gates JR, Fangman MC (1997) A reconsideration of bilateral language representation based on the intracarotid amobarbital procedure. Brain Cognition 33:118–132
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
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
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
Strauss E, Wada J (1983) Lateral preferences and cerebral speech dominance. Cortex 19:165–177
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
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
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
Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralisation of cerebral speech dominance. J Neurosurg 17:226–282
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
Whitehouse AJO, Bishop DVM (2009) Hemispheric division of function is the result of independent probabilistic biases. Neuropsychologia 47:1938–1943
Wilke M, Lidzba K (2007) LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods 163:128–136
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
Woods RP, Dodrill CB, Ojemann GA (1988) Brain injury, handedness, and speech lateralization in a series of amobarbital studies. Ann Neurol 23:510–518
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
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
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
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-015-1068-x