Age-related language lateralization assessed by fMRI: The effects of sex and handedness

Previous studies focusing on the relationship between lateralization of language function and age suffer from lack of a balanced distribution of age and handedness among participants, especially in the extremes of age. This limits our understanding of the influence of these factors on lateralization of language circuitry. The hemispheric asymmetry reduction in older adults (HAROLD) model suggests that under similar circumstances, involvement in cognitive processes of prefrontal (and potentially other) cortical areas tends to be less lateralized with age. In this study, we aimed to investigate the link between age, gender, and language lateralization in a large group of healthy participants with a relatively even distribution of age and handedness in order to further test the HAROLD model. 99 healthy men (33 left-handed; age range 18-74years) and 125 women (44 left-handed; age range 19-76) were recruited. All participants underwent fMRI at 3T with a semantic decision and a verb generation tasks and received a battery of linguistic tests. Lateralization indexes (LI) were calculated for each participant based on fMRI results for each task separately. LIs were found to be significantly decreasing with age only in right-handed men and only in temporo-parietal cortical area. LIs did not change with age in other brain regions or in left-handed subjects. Our results do not support the HAROLD model and suggest a potentially different relationship between aging and lateralization of language functions.

[1]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[2]  C. Grady Cognitive Neuroscience of Aging , 2008, Annals of the New York Academy of Sciences.

[3]  R. E. Hicks,et al.  Pathological left-handedness and familial sinistrality in relation to degree of mental retardation , 1984, Brain and Cognition.

[4]  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.

[5]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[6]  V. Schmithorst,et al.  Cortical reorganization of language functioning following perinatal left MCA stroke , 2008, Brain and Language.

[7]  P. Maeder,et al.  Acute aphasia after right hemisphere stroke , 2009, Journal of Neurology.

[8]  J. Vannest,et al.  Age at stroke determines post-stroke language lateralization. , 2014, Restorative neurology and neuroscience.

[9]  T. Elmo Hemispheric asymmetry of auditory evoked potentials to comparisons within and across phonetic categories. , 1987, Scandinavian journal of psychology.

[10]  Kenneth Hugdahl,et al.  Sex differences in language asymmetry are age-dependent and small: A large-scale, consonant–vowel dichotic listening study with behavioral and fMRI data , 2013, Cortex.

[11]  I. Zucker,et al.  Sex bias in neuroscience and biomedical research , 2011, Neuroscience & Biobehavioral Reviews.

[12]  Roel M. Willems,et al.  On the other hand: including left-handers in cognitive neuroscience and neurogenetics , 2014, Nature Reviews Neuroscience.

[13]  Nina Kraus,et al.  Aging Affects Hemispheric Asymmetry in the Neural Representation of Speech Sounds , 2000, The Journal of Neuroscience.

[14]  J. Szaflarski,et al.  Different patterns of language activation in post-stroke aphasia are detected by overt and covert versions of the verb generation fMRI task , 2012, Medical science monitor : international medical journal of experimental and clinical research.

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

[16]  J. A. Frost,et al.  Language dominance in neurologically normal and epilepsy subjects , 1999 .

[17]  Vincent Schmithorst,et al.  A group independent component analysis of covert verb generation in children: A functional magnetic resonance imaging study , 2010, NeuroImage.

[18]  M. García-Fiñana,et al.  The effect of sex and handedness on white matter anisotropy: a diffusion tensor magnetic resonance imaging study , 2012, Neuroscience.

[19]  Jerzy P. Szaflarski,et al.  Females and males are highly similar in language performance and cortical activation patterns during verb generation , 2012, Cortex.

[20]  Jerzy P. Szaflarski,et al.  Right hemispheric participation in semantic decision improves performance , 2011, Brain Research.

[21]  R. Jacobs Computational studies of the development of functionally specialized neural modules , 1999, Trends in Cognitive Sciences.

[22]  Cheryl L. Grady,et al.  AGE-RELATED CHANGES IN THE NEURAL CORRELATES OF DEGRADED AND NONDEGRADED FACE PROCESSING , 2000, Cognitive neuropsychology.

[23]  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.

[24]  Xi-Nian Zuo,et al.  Regional Homogeneity , 2015, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[25]  D. Plaut,et al.  Complementary neural representations for faces and words: A computational exploration , 2011, Cognitive neuropsychology.

[26]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[27]  X. Zuo,et al.  Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: A systems neuroscience perspective , 2014, Neuroscience & Biobehavioral Reviews.

[28]  R. Buckner,et al.  Does the right hemisphere take over after damage to Broca’s area? the Barlow case of 1877 and its history , 2003, Brain and Language.

[29]  Jonathan M. Campbell,et al.  Peabody Picture Vocabulary Test , 2010 .

[30]  Huafu Chen,et al.  Disrupted Intrinsic Local Synchronization in Poststroke Aphasia , 2016, Medicine.

[31]  Karl J. Friston,et al.  Cerebral Asymmetry and the Effects of Sex and Handedness on Brain Structure: A Voxel-Based Morphometric Analysis of 465 Normal Adult Human Brains , 2001, NeuroImage.

[32]  M. Rugg,et al.  The relationship between aging, performance, and the neural correlates of successful memory encoding. , 2009, Cerebral cortex.

[33]  P. Greenwood Functional plasticity in cognitive aging: review and hypothesis. , 2007, Neuropsychology.

[34]  Vincent J Schmithorst,et al.  fMRI Shows Atypical Language Lateralization in Pediatric Epilepsy Patients , 2006, Epilepsia.

[35]  Yufeng Zang,et al.  DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging , 2016, Neuroinformatics.

[36]  L. M. Sacheli,et al.  With time on our side? Task-dependent compensatory processes in graceful aging , 2010, Experimental Brain Research.

[37]  A. Friederici The brain basis of language processing: from structure to function. , 2011, Physiological reviews.

[38]  Abraham Z. Snyder,et al.  A method for using blocked and event-related fMRI data to study “resting state” functional connectivity , 2007, NeuroImage.

[39]  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.

[40]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[41]  Jerzy P. Szaflarski,et al.  Semantic association investigated with functional MRI and independent component analysis , 2011, Epilepsy & Behavior.

[42]  Cheryl L. Grady,et al.  The effects of encoding task on age-related differences in the functional neuroanatomy of face memory. , 2002, Psychology and aging.

[43]  William H Theodore,et al.  Practice guideline summary: Use of fMRI in the presurgical evaluation of patients with epilepsy , 2017, Neurology.

[44]  B. Turetsky,et al.  Sex differences in aging of the human frontal and temporal lobes , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  Jerzy P. Szaflarski,et al.  Left-handedness and language lateralization in children , 2012, Brain Research.

[46]  C. Miniussi,et al.  Successful physiological aging and episodic memory: A brain stimulation study , 2011, Behavioural Brain Research.

[47]  C. Nelson,et al.  The lateralization of language comprehension using event-related potentials , 1990, Brain and Cognition.

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

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

[50]  Jerzy P. Szaflarski,et al.  Comprehensive presurgical functional MRI language evaluation in adult patients with epilepsy , 2008, Epilepsy & Behavior.

[51]  J. Vannest,et al.  The effects of temporal lobe epilepsy on scene encoding , 2013, Epilepsy & Behavior.

[52]  Joseph C. Griffis,et al.  Voxel-based Gaussian naïve Bayes classification of ischemic stroke lesions in individual T1-weighted MRI scans , 2016, Journal of Neuroscience Methods.

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

[54]  Scott Holland,et al.  Reliability of fMRI for studies of language in post-stroke aphasia subjects , 2008, NeuroImage.

[55]  Claudio Babiloni,et al.  Age-Related Functional Changes of Prefrontal Cortex in Long-Term Memory: A Repetitive Transcranial Magnetic Stimulation Study , 2004, The Journal of Neuroscience.

[56]  M. Kendall,et al.  Rank Correlation Methods , 1949 .

[57]  M. Caulo,et al.  Multimodal assessment of hemispheric lateralization for language and its relevance for behavior , 2016, NeuroImage.

[58]  S. Kosslyn Seeing and imagining in the cerebral hemispheres: a computational approach. , 1987, Psychological review.

[59]  Yufeng Zang,et al.  Toward reliable characterization of functional homogeneity in the human brain: Preprocessing, scan duration, imaging resolution and computational space , 2013, NeuroImage.

[60]  Charles J. Wysocki,et al.  Hand preference and age in the United States , 1992, Neuropsychologia.

[61]  Rodolphe Nenert,et al.  Arcuate fasciculus asymmetry has a hand in language function but not handedness , 2016, Human brain mapping.

[62]  C. Cullum,et al.  Generative naming in normal aging: Total output and qualitative changes using phonemic and semantic constraints , 1995 .

[63]  T. Olsen,et al.  Aphasia in acute stroke: Incidence, determinants, and recovery , 1995, Annals of neurology.

[64]  Daniel P. Jones,et al.  Twenty years and still counting: including women as participants and studying sex and gender in biomedical research , 2015, BMC Women's Health.

[65]  V. Schmithorst,et al.  fMRI study of language lateralization in children and adults , 2006, Human brain mapping.

[66]  M. Annett Handedness and the cerebral representation of speech. , 1976, Annals of Human Biology.

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

[68]  Yingli Lu,et al.  Regional homogeneity approach to fMRI data analysis , 2004, NeuroImage.

[69]  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 .

[70]  J. Babb,et al.  Age-related total gray matter and white matter changes in normal adult brain. Part I: volumetric MR imaging analysis. , 2002, AJNR. American journal of neuroradiology.

[71]  E. Paulesu,et al.  Reassessing the HAROLD model: Is the hemispheric asymmetry reduction in older adults a special case of compensatory-related utilisation of neural circuits? , 2013, Experimental Brain Research.

[72]  Yufeng Zang,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010 .

[73]  H. Urbach,et al.  Clinical and neuropsychological characteristics of pediatric epilepsy patients with atypical language dominance , 2003, Epilepsy & Behavior.

[74]  E. T. Possing,et al.  Language lateralization in left-handed and ambidextrous people: fMRI data , 2002, Neurology.

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

[76]  E. Kaplan,et al.  The Boston naming test , 2001 .

[77]  S. Small,et al.  Interhemispheric Functional Connectivity following Prenatal or Perinatal Brain Injury Predicts Receptive Language Outcome , 2013, The Journal of Neuroscience.

[78]  M. Corballis The evolution and genetics of cerebral asymmetry , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.