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

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

[1]  Robert J. Zatorre,et al.  Perceptual asymmetry on the dichotic fused words test and cerebral speech lateralization determined by the carotid sodium amytal test , 1989, Neuropsychologia.

[2]  Angela D. Friederici,et al.  Non-invasive regime for language lateralization in right and left-handers by means of functional MRI and dichotic listening , 2002, Experimental Brain Research.

[3]  Roel M. Willems,et al.  Add a picture for suspense: neural correlates of the interaction between language and visual information in the perception of fear. , 2011, Social cognitive and affective neuroscience.

[4]  Tobias Loddenkemper,et al.  Atypical language lateralization in epilepsy patients , 2009, Epilepsia.

[5]  E. Ritzl,et al.  Characterization of atypical language activation patterns in focal epilepsy , 2014, Annals of neurology.

[6]  Alan C. Evans,et al.  Growing Together and Growing Apart: Regional and Sex Differences in the Lifespan Developmental Trajectories of Functional Homotopy , 2010, The Journal of Neuroscience.

[7]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[8]  Amos Storkey,et al.  18th Annual Meeting of the Organization for Human Brain Mapping , 2012 .

[9]  S. Small,et al.  Left hemisphere regions are critical for language in the face of early left focal brain injury. , 2010, Brain : a journal of neurology.

[10]  Michael L Lipton,et al.  Note: This Copy Is for Your Personal, Non-commercial Use Only. to Order Presentation-ready Copies for Distribution to Your Colleagues or Clients, Contact Us at Www.rsna.org/rsnarights. Materials and Methods , 2022 .

[11]  Tim B. Dyrby,et al.  Orientationally invariant indices of axon diameter and density from diffusion MRI , 2010, NeuroImage.

[12]  Mitchel S Berger,et al.  Homotopic organization of essential language sites in right and bilateral cerebral hemispheric dominance. , 2011, Journal of neurosurgery.

[13]  E. Ringelstein,et al.  Handedness and hemispheric language dominance in healthy humans. , 2000, Brain : a journal of neurology.

[14]  G. Ojemann,et al.  Atypical speech is rare in individuals with normal developmental histories , 2003, Neurology.

[15]  Cathy J Price,et al.  The latest on functional imaging studies of aphasic stroke , 2005, Current opinion in neurology.

[16]  Jeffrey R. Binder,et al.  Functional MRI is a valid noninvasive alternative to Wada testing , 2011, Epilepsy & Behavior.

[17]  Dorothy V.M. Bishop,et al.  No population bias to left-hemisphere language in 4-year-olds with language impairment , 2014, PeerJ.

[18]  T. Rasmussen,et al.  INTRACAROTID SODIUM AMYTAL FOR THE LATERALIZATION OF CEREBRAL SPEECH DOMINANCE; OBSERVATIONS IN 123 PATIENTS. , 1964, Journal of neurosurgery.

[19]  L. Knaap,et al.  How does the corpus callosum mediate interhemispheric transfer? A review , 2011, Behavioural Brain Research.

[20]  Marc Joliot,et al.  Gaussian Mixture Modeling of Hemispheric Lateralization for Language in a Large Sample of Healthy Individuals Balanced for Handedness , 2014, PloS one.

[21]  J. Talairach,et al.  Hemispheric lateralization of motor and speech functions after early brain lesion: Study of 73 epileptic patients with intracarotid amytal test , 1988, Neuropsychologia.

[22]  Mateer Ca,et al.  Neuropsychological and linguistic correlates of atypical language lateralization: evidence from sodium amytal studies. , 1983 .

[23]  E. Strauss,et al.  Lateral Preferences and Cerebral Speech Dominance , 1983, Cortex.

[24]  Orrin Devinsky,et al.  Degree of handedness and cerebral dominance , 2006, Neurology.

[25]  G. Ojemann,et al.  Cortical stimulation mapping and Wada results demonstrate a normal variant of right hemisphere language organization , 2012, Epilepsia.

[26]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[27]  M. Corbetta,et al.  Neural correlates of recovery from aphasia after damage to left inferior frontal cortex , 2000, Neurology.

[28]  R. Woods,et al.  Recovery from wernicke's aphasia: A positron emission tomographic study , 1995, Annals of neurology.

[29]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[30]  C B Dodrill,et al.  Brain injury, handedness, and speech lateralization in a series of amobarbital studies , 1988, Annals of neurology.

[31]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[32]  D. Bishop,et al.  Hemispheric division of function is the result of independent probabilistic biases , 2009, Neuropsychologia.

[33]  John B. Dillon Left Handedness , 1914, Science.

[34]  B. Mazoyer,et al.  Revisiting human hemispheric specialization with neuroimaging , 2013, Trends in Cognitive Sciences.

[35]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[36]  H. Hécaen,et al.  Cerebral organization in left-handers , 1981, Brain and Language.

[37]  H Hécaen,et al.  Cerebral dominance in left-handed subjects. , 1971, Cortex; a journal devoted to the study of the nervous system and behavior.

[38]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[39]  D. Margulies,et al.  Regional Variation in Interhemispheric Coordination of Intrinsic Hemodynamic Fluctuations , 2008, The Journal of Neuroscience.

[40]  W. Gardner,et al.  Embryonal atresia of the fourth ventricle. The cause of "arachnoid cyst" of the cerebellopontine angle. , 1960, Journal of neurosurgery.

[41]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[42]  Bernard Mazoyer,et al.  What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis , 2011, NeuroImage.

[43]  Chun-Hung Yeh,et al.  Probabilistic topography of human corpus callosum using cytoarchitectural parcellation and high angular resolution diffusion imaging tractography , 2009, Human brain mapping.

[44]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[45]  M. Annett Handedness and cerebral dominance: the right shift theory. , 1998, The Journal of neuropsychiatry and clinical neurosciences.

[46]  Jorge Sepulcre,et al.  Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors , 2009, Proceedings of the National Academy of Sciences.

[47]  M. Gazzaniga Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? , 2000, Brain : a journal of neurology.

[48]  Suman Jayadev,et al.  Gender differences in handedness and speech lateralization related to early neurologic insults , 2005, Neurology.

[49]  Marko Wilke,et al.  LI-tool: A new toolbox to assess lateralization in functional MR-data , 2007, Journal of Neuroscience Methods.

[50]  C. Mateer,et al.  Neuropsychological and linguistic correlates of atypical language lateralization: evidence from sodium amytal studies. , 1983, Human neurobiology.

[51]  J. Pujol,et al.  Cerebral lateralization of language in normal left-handed people studied by functional MRI , 1999, Neurology.

[52]  I. V. D. van der Ham,et al.  How does the corpus callosum mediate interhemispheric transfer? A review. , 2011, Behavioural brain research.

[53]  D. Perani,et al.  A fMRI study of word retrieval in aphasia , 2003, Brain and Language.

[54]  B Milner,et al.  THE ROLE OF EARLY LEFT‐BRAIN INJURY IN DETERMINING LATERALIZATION OF CEREBRAL SPEECH FUNCTIONS , 1977, Annals of the New York Academy of Sciences.

[55]  J. Gates,et al.  A Reconsideration of Bilateral Language Representation Based on the Intracarotid Amobarbital Procedure , 1997, Brain and Cognition.

[56]  Angela D Friederici,et al.  The language network , 2012, Current Opinion in Neurobiology.

[57]  Bernard Mazoyer,et al.  BIL&GIN: A neuroimaging, cognitive, behavioral, and genetic database for the study of human brain lateralization , 2016, NeuroImage.

[58]  T. Rasmussen,et al.  INTRACAROTID INJECTION OF SODIUM AMYTAL FOR THE LATERALIZATION OF CEREBRAL SPEECH DOMINANCE EXPERIMENTAL AND CLINICAL OBSERVATIONS , 1960 .