Verbal Fluency Is Affected by Altered Brain Lateralization in Adults Who Were Born Very Preterm

Abstract Language difficulties have been reported in children and adolescents who were born very preterm (<32 weeks’ gestation) and associated with an atypical lateralization of language processing, i.e., increased right-hemispheric engagement. This study used functional magnetic resonance imaging (fMRI) and spherical deconvolution tractography to study the hemodynamic responses associated with verbal fluency processing (easy and hard letter trials) and verbal fluency-related white matter fiber tracts in 64 very preterm born adults and 36 adult controls (mean age: 30 years). Tractography of the arcuate fasciculus (AF) and frontal aslant tract (FAT) was performed. Tracts were quantified in terms of mean volume, hindrance modulated orientational anisotropy, and lateralization, assessed using a laterality index (LI) to indicate hemispheric dominance. During verbal fluency fMRI, very preterm participants displayed decreased hemodynamic response suppression in both the Easy > Rest and Hard > Rest conditions, compared to controls, in superior temporal gyrus (STG), insula, thalamus, and sensorimotor cortex, particularly in the right hemisphere. At the whole-group level, decreased hemodynamic response suppression in the right sensorimotor cortex was associated with worse on-line performance on the hard letter trials. Increased left-laterality in the AF was present alongside increased right hemispheric hemodynamic response suppression in controls. When only right-handed participants were considered, decreased hemodynamic response suppression in the right STG during hard letter trials was related to weaker left and right FAT white matter integrity in the preterm group only. These results show that verbal fluency is affected by altered functional lateralization in adults who were born very preterm.

[1]  Albert Gjedde,et al.  Putative Tests of Frontal Lobe Function: A PET-Study of Brain Activation During Stroop's Test and Verbal Fluency , 2002, Journal of clinical and experimental neuropsychology.

[2]  G. Hickok,et al.  AuditoryMotor Interaction Revealed by fMRI: Speech, Music, and Working Memory in Area Spt , 2003, Journal of Cognitive Neuroscience.

[3]  Gary Glover,et al.  Developmental Cognitive Neuroscience Differences in Neural Activation between Preterm and Full Term Born Adolescents on a Sentence Comprehension Task: Implications for Educational Accommodations , 2022 .

[4]  Oren Civier,et al.  The frontal aslant tract underlies speech fluency in persistent developmental stuttering , 2014, Brain Structure and Function.

[5]  R. Kikinis,et al.  Quantitative magnetic resonance imaging of brain development in premature and mature newborns , 1998, Annals of neurology.

[6]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[7]  P. Marschik,et al.  Differences between girls and boys in emerging language skills: evidence from 10 language communities. , 2012, The British journal of developmental psychology.

[8]  R. Murray,et al.  Functional Neuroanatomy of Executive Function after Neonatal Brain Injury in Adults Who Were Born Very Preterm , 2014, PloS one.

[9]  Giuseppe Scotti,et al.  A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution , 2010, NeuroImage.

[10]  Dustin Scheinost,et al.  Cerebral Lateralization is Protective in the Very Prematurely Born. , 2015, Cerebral cortex.

[11]  Colin Studholme,et al.  Early folding patterns and asymmetries of the normal human brain detected from in utero MRI. , 2012, Cerebral cortex.

[12]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[13]  Roy H. Hamilton,et al.  The right hemisphere is not unitary in its role in aphasia recovery , 2012, Cortex.

[14]  A. Toga,et al.  Mapping sulcal pattern asymmetry and local cortical surface gray matter distribution in vivo: maturation in perisylvian cortices. , 2002, Cerebral cortex.

[15]  Lucie Hertz-Pannier,et al.  Nature and nurture in language acquisition: anatomical and functional brain-imaging studies in infants , 2006, Trends in Neurosciences.

[16]  Chiara Nosarti,et al.  Preterm birth and structural brain alterations in early adulthood , 2014, NeuroImage: Clinical.

[17]  D. Tomasi,et al.  Common deactivation patterns during working memory and visual attention tasks: An intra‐subject fMRI study at 4 Tesla , 2006, Human brain mapping.

[18]  D. Bishop.  Cerebral Asymmetry and Language Development: Cause, Correlate, or Consequence? , 2013, Science.

[19]  Michel Thiebaut de Schotten,et al.  Short frontal lobe connections of the human brain , 2012, Cortex.

[20]  T. Crow,et al.  Right hemisphere language functions and schizophrenia: the forgotten hemisphere? , 2005, Brain : a journal of neurology.

[21]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[22]  Friedemann Pulvermüller,et al.  Brain mechanisms linking language and action , 2005, Nature Reviews Neuroscience.

[23]  J. Oosterlaan,et al.  Meta-Analysis of Neurobehavioral Outcomes in Very Preterm and/or Very Low Birth Weight Children , 2009, Pediatrics.

[24]  Núria Bargalló,et al.  Correlations of thalamic reductions with verbal fluency impairment in those born prematurely , 2006, Neuroreport.

[25]  Daniel Rueckert,et al.  Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry , 2006, NeuroImage.

[26]  Alexander Leemans,et al.  The B‐matrix must be rotated when correcting for subject motion in DTI data , 2009, Magnetic resonance in medicine.

[27]  M Deppe,et al.  Behavioural relevance of atypical language lateralization in healthy subjects. , 2001, Brain : a journal of neurology.

[28]  Jan Sijbers,et al.  ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data , 2009 .

[29]  Chiara Nosarti,et al.  Alterations in cortical thickness development in preterm-born individuals: Implications for high-order cognitive functions , 2015, NeuroImage.

[30]  Alex Martin,et al.  Neural systems supporting lexical search guided by letter and semantic category cues: A self-paced overt response fMRI study of verbal fluency , 2010, NeuroImage.

[31]  Angela D. Friederici,et al.  The ontogeny of the cortical language network , 2016, Nature Reviews Neuroscience.

[32]  Chiara Nosarti,et al.  White matter alterations to cingulum and fornix following very preterm birth and their relationship with cognitive functions , 2017, NeuroImage.

[33]  J. Allsop,et al.  Thalamocortical Connectivity Predicts Cognition in Children Born Preterm , 2015, Cerebral cortex.

[34]  Angela D. Friederici,et al.  Maturation of the Language Network: From Inter- to Intrahemispheric Connectivities , 2011, PloS one.

[35]  Steen Moeller,et al.  ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging , 2014, NeuroImage.

[36]  Dustin Scheinost,et al.  Adaptive mechanisms of developing brain: Cerebral lateralization in the prematurely-born , 2015, NeuroImage.

[37]  Karl J. Friston,et al.  A PET study of word finding , 1991, Neuropsychologia.

[38]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[39]  M. Catani,et al.  Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true‐tract specific index to characterize white matter diffusion , 2013, Human brain mapping.

[40]  N. Volkow,et al.  Functional connectivity and brain activation: a synergistic approach. , 2014, Cerebral cortex.

[41]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[42]  Chiara Nosarti,et al.  Reinforcement of the Brain's Rich-Club Architecture Following Early Neurodevelopmental Disruption Caused by Very Preterm Birth , 2016, Cerebral cortex.

[43]  David A. Medler,et al.  Cerebral Cortex doi:10.1093/cercor/bhi040 Cerebral Cortex Advance Access published February 9, 2005 , 2022 .

[44]  G. Hickok,et al.  Auditory–Motor Interaction Revealed by fMRI: Speech, Music, and Working Memory in Area Spt , 2003 .

[45]  M. Jenkinson.  Non-linear registration aka Spatial normalisation , 2007 .

[46]  S. Teipel,et al.  Is the left uncinate fasciculus associated with verbal fluency decline in mild Alzheimer's disease? , 2016, Translational neuroscience.

[47]  D. Bishop,et al.  Atypical cerebral lateralisation in adults with compensated developmental dyslexia demonstrated using functional transcranial Doppler ultrasound , 2009, Brain and Language.

[48]  B. Wandell,et al.  The vertical occipital fasciculus: A century of controversy resolved by in vivo measurements , 2014, Proceedings of the National Academy of Sciences.

[49]  M. Sigman,et al.  Functional organization of perisylvian activation during presentation of sentences in preverbal infants , 2006, Proceedings of the National Academy of Sciences.

[50]  P. Karunanayaka,et al.  Functional MRI of language lateralization during development in children , 2007, International journal of audiology.

[51]  P Lestage,et al.  Verbal fluency output in children aged 7–16 as a function of the production criterion: Qualitative analysis of clustering, switching processes, and semantic network exploitation , 2004, Brain and Language.

[52]  M. Catani,et al.  A novel frontal pathway underlies verbal fluency in primary progressive aphasia. , 2013, Brain : a journal of neurology.

[53]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[54]  J. Volpe.  Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances , 2009, The Lancet Neurology.

[55]  Kayoko Okada,et al.  Area Spt in the Human Planum Temporale Supports Sensory-motor Integration for Speech Processing Establishing the Existence of Distinct Sen- Sory versus Motor Activation Patterns Would Establish That , 2022 .

[56]  G. Šimić,et al.  Extraordinary neoteny of synaptic spines in the human prefrontal cortex , 2011, Proceedings of the National Academy of Sciences.

[57]  B. Vohr,et al.  Alterations in functional connectivity for language in prematurely born adolescents , 2009, Brain : a journal of neurology.

[58]  Philip J. Brittain,et al.  Real-Life Impact of Executive Function Impairments in Adults Who Were Born Very Preterm , 2017, Journal of the International Neuropsychological Society.

[59]  B. Pearce,et al.  Autism, lateralisation, and handedness: A review of the literature and meta-analysis , 2014, Laterality.

[60]  Mohamed L. Seghier,et al.  Laterality index in functional MRI: methodological issues☆ , 2008, Magnetic resonance imaging.

[61]  F. Ehlen,et al.  Functional roles of the thalamus for language capacities , 2013, Front. Syst. Neurosci..

[62]  Brian A. Wandell,et al.  Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections , 2013, Brain and Language.

[63]  G. Langs,et al.  The prenatal origin of hemispheric asymmetry: an in utero neuroimaging study. , 2011, Cerebral cortex.

[64]  A. Snyder,et al.  Longitudinal analysis of neural network development in preterm infants. , 2010, Cerebral cortex.

[65]  N. Jovanov-Milošević,et al.  The development of cerebral connections during the first 20-45 weeks' gestation. , 2006, Seminars in fetal & neonatal medicine.

[66]  T. Q. Irigaray,et al.  Intellectual abilities in Alzheimer's disease patients: Contributions from the Wechsler Abbreviated Scale of Intelligence (WASI) , 2010 .

[67]  R. Murray,et al.  Very Early Brain Damage Leads to Remodeling of the Working Memory System in Adulthood: A Combined fMRI/Tractography Study , 2015, Journal of Neuroscience.

[68]  P. Maeder,et al.  Chronic cognitive impairment following laterothalamic infarcts: a study of 9 cases. , 2003, Archives of neurology.

[69]  Valentina Bambini,et al.  A model for Social Communication And Language Evolution and Development (SCALED) , 2014, Current Opinion in Neurobiology.

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

[71]  L. Fadiga,et al.  Active perception: sensorimotor circuits as a cortical basis for language , 2010, Nature Reviews Neuroscience.

[72]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[73]  Matthew F Glasser,et al.  DTI tractography of the human brain's language pathways. , 2008, Cerebral cortex.

[74]  Alan Connelly,et al.  Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution , 2004, NeuroImage.

[75]  B. Vohr,et al.  Evidence for Catch-up in Cognition and Receptive Vocabulary Among Adolescents Born Very Preterm , 2011, Pediatrics.

[76]  Michelle Hampson,et al.  Functional connectivity to a right hemisphere language center in prematurely born adolescents , 2010, NeuroImage.

[77]  Michelle Hampson,et al.  Preterm birth results in alterations in neural connectivity at age 16 years , 2011, NeuroImage.

[78]  M. Annett.  The Binomial Distribution of Right, Mixed and Left Handedness , 1967, The Quarterly journal of experimental psychology.

[79]  Natasha Lepore,et al.  Fiber estimation and tractography in diffusion MRI: Development of simulated brain images and comparison of multi-fiber analysis methods at clinical b-values , 2015, NeuroImage.

[80]  Zhishun Wang,et al.  Visual inspection of independent components: Defining a procedure for artifact removal from fMRI data , 2010, Journal of Neuroscience Methods.

[81]  D. Haas.  Preterm birth. , 2011, BMJ clinical evidence.

[82]  Byron Bernal,et al.  Participation of the insula in language revisited: A meta-analytic connectivity study , 2014, Journal of Neurolinguistics.

[83]  D. Le Bihan,et al.  Structural Asymmetries in the Infant Language and Sensori-motor Networks , 2022 .

[84]  Pascale Tremblay,et al.  Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. , 2012, Brain : a journal of neurology.

[85]  Philip K. McGuire,et al.  A Functional Magnetic Resonance Imaging Study of Overt Letter Verbal Fluency Using a Clustered Acquisition Sequence: Greater Anterior Cingulate Activation with Increased Task Demand , 2002, NeuroImage.

[86]  Chiara Nosarti,et al.  Neural substrates of letter fluency processing in young adults who were born very preterm: Alterations in frontal and striatal regions , 2009, NeuroImage.

[87]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[88]  R. Murray,et al.  A multimodal imaging study of recognition memory in very preterm born adults , 2016, Human brain mapping.

[89]  Jason D. Yeatman,et al.  Language and reading skills in school-aged children and adolescents born preterm are associated with white matter properties on diffusion tensor imaging , 2012, Neuropsychologia.

[90]  C. Nosarti,et al.  Developments in diffusion MRI and tractography to study language network alterations following very preterm birth , 2018 .

[91]  Chiara Nosarti,et al.  Preterm birth and psychiatric disorders in young adult life. , 2012, Archives of general psychiatry.

[92]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[93]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[94]  Ludovica Griffanti,et al.  Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers , 2014, NeuroImage.

[95]  M. Just,et al.  From the Selectedworks of Marcel Adam Just the Organization of Thinking: What Functional Brain Imaging Reveals about the Neuroarchitecture of Complex Cognition , 2022 .

[96]  E. Reynolds,et al.  Ultrasound appearance of the brain in very preterm infants and neurodevelopmental outcome at 18 months of age. , 1983, Archives of disease in childhood.

[97]  Walter Schneider,et al.  Co-analysis of brain structure and function using fMRI and diffusion-weighted imaging. , 2012, Journal of visualized experiments : JoVE.

[98]  Michelle Hampson,et al.  Alterations in neural connectivity in preterm children at school age , 2009, NeuroImage.

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