A coordinate-based ALE functional MRI meta-analysis of brain activation during verbal fluency tasks in healthy control subjects

BackgroundThe processing of verbal fluency tasks relies on the coordinated activity of a number of brain areas, particularly in the frontal and temporal lobes of the left hemisphere. Recent studies using functional magnetic resonance imaging (fMRI) to study the neural networks subserving verbal fluency functions have yielded divergent results especially with respect to a parcellation of the inferior frontal gyrus for phonemic and semantic verbal fluency. We conducted a coordinate-based activation likelihood estimation (ALE) meta-analysis on brain activation during the processing of phonemic and semantic verbal fluency tasks involving 28 individual studies with 490 healthy volunteers.ResultsFor phonemic as well as for semantic verbal fluency, the most prominent clusters of brain activation were found in the left inferior/middle frontal gyrus (LIFG/MIFG) and the anterior cingulate gyrus. BA 44 was only involved in the processing of phonemic verbal fluency tasks, BA 45 and 47 in the processing of phonemic and semantic fluency tasks.ConclusionsOur comparison of brain activation during the execution of either phonemic or semantic verbal fluency tasks revealed evidence for spatially different activation in BA 44, but not other regions of the LIFG/LMFG (BA 9, 45, 47) during phonemic and semantic verbal fluency processing.

[1]  G. Eden,et al.  Examining the Central and Peripheral Processes of Written Word Production Through Meta-Analysis , 2011, Front. Psychology.

[2]  S C Williams,et al.  Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. , 1997, Magnetic resonance imaging.

[3]  Simon B. Eickhoff,et al.  Specialisation in Broca's region for semantic, phonological, and syntactic fluency? , 2008, NeuroImage.

[4]  Michael J Brammer,et al.  Functional magnetic resonance imaging of verbal fluency and confrontation naming using compressed image acquisition to permit overt responses , 2003, Human brain mapping.

[5]  G. Oberg,et al.  Cross‐linguistic meta‐analysis of phonological fluency: Normal performance across cultures , 2006 .

[6]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[7]  Sophie Schwartz,et al.  Distinct patterns of word retrieval in right and left frontal lobe patients: a multidimensional perspective , 2001, Neuropsychologia.

[8]  E. Phelps,et al.  FMRI of the prefrontal cortex during overt verbal fluency , 1997, Neuroreport.

[9]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2010, International journal of surgery.

[10]  Kathryn M. McMillan,et al.  A comparison of label‐based review and ALE meta‐analysis in the Stroop task , 2005, Human brain mapping.

[11]  Marcus Meinzer,et al.  Neural Signatures of Semantic and Phonemic Fluency in Young and Old Adults , 2009, Journal of Cognitive Neuroscience.

[12]  Sharon L. Thompson-Schill,et al.  Prefrontal Cortical Response to Conflict during Semantic and Phonological Tasks , 2007, Journal of Cognitive Neuroscience.

[13]  Sergi Costafreda-Gonzalez Parametric coordinate-based meta-analysis: valid effect size meta-analysis of studies with differing statistical thresholds , 2012 .

[14]  C. Kremser,et al.  Brain activation pattern during a verbal fluency test in healthy male and female volunteers: a functional magnetic resonance imaging study , 2003, Neuroscience Letters.

[15]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[16]  Simon B. Eickhoff,et al.  Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—The roles of Brodmann areas 44 and 45 , 2004, NeuroImage.

[17]  J. Petrella,et al.  Developmental aspects of language processing: fMRI of verbal fluency in children and adults , 2003, Human brain mapping.

[18]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[19]  Peter Q. Pfordresher,et al.  The somatotopy of speech: Phonation and articulation in the human motor cortex , 2009, Brain and Cognition.

[20]  Perrine Ruby,et al.  A relation between rest and the self in the brain? , 2003, Brain Research Reviews.

[21]  M. Bates,et al.  FAS and CFL Forms of Verbal Fluency Differ in Difficulty: A Meta-analytic Study , 2008, Applied neuropsychology.

[22]  A. Georgi,et al.  Genetic variation in G72 correlates with brain activation in the right middle temporal gyrus in a verbal fluency task in healthy individuals , 2011, Human brain mapping.

[23]  T. Tombaugh,et al.  Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. , 1999, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[24]  Angela R. Laird,et al.  Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation , 2011, NeuroImage.

[25]  M E Meyerand,et al.  Reliability of functional MR imaging with word-generation tasks for mapping Broca's area. , 2001, AJNR. American journal of neuroradiology.

[26]  Philippe Lahorte,et al.  Verbal fluency as a prefrontal activation probe: a validation study using 99mTc-ECD brain SPET , 2000, European Journal of Nuclear Medicine.

[27]  J. T. Lurito,et al.  Comparison of Rhyming and Word Generation with FMRI , 1998, NeuroImage.

[28]  J. Stokholm,et al.  Performances on five verbal fluency tests in a healthy, elderly Danish sample , 2013, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[29]  M J Brammer,et al.  Attenuated frontal activation during a verbal fluency task in patients with schizophrenia. , 1998, The American journal of psychiatry.

[30]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[31]  S. Thompson-Schill Neuroimaging studies of semantic memory: inferring “how” from “where” , 2003, Neuropsychologia.

[32]  Keith M. McGregor,et al.  Impact of changed positive and negative task-related brain activity on word-retrieval in aging , 2012, Neurobiology of Aging.

[33]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

[34]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[35]  H. Coslett,et al.  Localization of sublexical speech perception components , 2010, Brain and Language.

[36]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[37]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[38]  Brian Everitt,et al.  A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus , 2006, Human brain mapping.

[39]  A. Lundervold,et al.  Left frontal activation during a semantic categorization task: an fMRI-study. , 1999, The International journal of neuroscience.

[40]  J. Lewin,et al.  Brain Activation During Silent Word Generation Evaluated with Functional MRI , 1998, Brain and Language.

[41]  Richard S. J. Frackowiak,et al.  Noun and verb retrieval by normal subjects. Studies with PET. , 1996, Brain : a journal of neurology.

[42]  J. Jolles,et al.  Normative data for the Animal, Profession and Letter M Naming verbal fluency tests for Dutch speaking participants and the effects of age, education, and sex , 2006, Journal of the International Neuropsychological Society.

[43]  Ralph-Axel Müller,et al.  Category-specific activations during word generation reflect experiential sensorimotor modalities , 2009, NeuroImage.

[44]  S A Spence,et al.  No evidence for left superior temporal dysfunction in asymptomatic schizophrenia and bipolar disorder , 1999, British Journal of Psychiatry.

[45]  Daphne Bavelier,et al.  Dissociating neural subsystems for grammar by contrasting word order and inflection , 2010, Proceedings of the National Academy of Sciences.

[46]  J. Henry,et al.  A Meta-Analytic Review of Verbal Fluency Deficits in Depression , 2005, Journal of clinical and experimental neuropsychology.

[47]  Michael L. Hines,et al.  Neuroinformatics Original Research Article Neuron and Python , 2022 .

[48]  BMC Neuroscience , 2003 .

[49]  Angela R. Laird,et al.  Activation likelihood estimation meta-analysis revisited , 2012, NeuroImage.

[50]  K. Amunts,et al.  Posterior parietal cortex is implicated in continuous switching between verbal fluency tasks: an fMRI study with clinical implications , 2002 .

[51]  Laure Zago,et al.  How verbal and spatial manipulation networks contribute to calculation: An fMRI study , 2008, Neuropsychologia.

[52]  Stefan Knecht,et al.  How atypical is atypical language dominance? , 2003, NeuroImage.

[53]  Y. Okamoto,et al.  Attenuated Left Prefrontal Activation during a Verbal Fluency Task in Patients with Depression , 2003, Neuropsychobiology.

[54]  A P Shimamura,et al.  Verbal and design fluency in patients with frontal lobe lesions , 2001, Journal of the International Neuropsychological Society.

[55]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[56]  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.

[57]  Arthur L. Benton,et al.  Word fluency and brain damage , 1967 .

[58]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[59]  S. Golaszewski,et al.  Brain activation patterns during a verbal fluency test—a functional MRI study in healthy volunteers and patients with schizophrenia , 2004, Schizophrenia Research.

[60]  A. Simmons,et al.  Comparable fMRI activity with differential behavioural performance on mental rotation and overt verbal fluency tasks in healthy men and women , 2006, Experimental Brain Research.

[61]  John S. Duncan,et al.  Hippocampal activation correlates with visual confrontation naming: fMRI findings in controls and patients with temporal lobe epilepsy , 2011, Epilepsy Research.

[62]  J. Henry,et al.  Covariates of Production and Perseveration on Tests of Phonemic, Semantic and Alternating Fluency in Normal Aging , 2006, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[63]  V M Haughton,et al.  A comparison of functional MR activation patterns during silent and audible language tasks. , 1995, AJNR. American journal of neuroradiology.

[64]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[65]  Ralph-Axel Müller,et al.  Effects of generation mode in fMRI adaptations of semantic fluency: Paced production and overt speech , 2007, Neuropsychologia.

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

[67]  Iain D. Gilchrist,et al.  Testing a Simplified Method for Measuring Velocity Integration in Saccades Using a Manipulation of Target Contrast , 2011, Front. Psychology.

[68]  Simon B Eickhoff,et al.  Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses , 2012, Human brain mapping.

[69]  G. K. Henry,et al.  Verbal fluency task equivalence , 1996 .

[70]  M. Duyme,et al.  Sex and performance level effects on brain activation during a verbal fluency task: A functional magnetic resonance imaging study , 2009, Cortex.

[71]  S. Petersen,et al.  A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging , 2003, Neuropsychologia.

[72]  Tilo Kircher,et al.  Task-dependent Modulations of Prefrontal and Hippocampal Activity during Intrinsic Word Production , 2009, Journal of Cognitive Neuroscience.

[73]  R. E. Gur,et al.  Effect of retrieval effort and switching demand on fMRI activation during semantic word generation in schizophrenia , 2008, Schizophrenia Research.

[74]  R. Buckner,et al.  Common Prefrontal Regions Coactivate with Dissociable Posterior Regions during Controlled Semantic and Phonological Tasks , 2002, Neuron.

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

[76]  Randy L Buckner,et al.  Common and dissociable activation patterns associated with controlled semantic and phonological processing: evidence from FMRI adaptation. , 2005, Cerebral cortex.

[77]  H. Rusinek,et al.  Functional magnetic resonance imaging of human brain activity in a verbal fluency task , 1998, Journal of neurology, neurosurgery, and psychiatry.

[78]  S. Bookheimer Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[79]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[80]  J. Fiez Phonology, Semantics, and the Role of the Left Inferior Prefrontal Cortex , 2022 .

[81]  M Hutchinson,et al.  Task-specific deactivation patterns in functional magnetic resonance imaging. , 1999, Magnetic resonance imaging.

[82]  Ioulia Kovelman,et al.  Bilingual and Monolingual Brains Compared: A Functional Magnetic Resonance Imaging Investigation of Syntactic Processing and a Possible Neural Signature of Bilingualism , 2008, Journal of Cognitive Neuroscience.

[83]  Arne Nagels,et al.  Neural correlates of rhyming vs. lexical and semantic fluency , 2011, Brain Research.

[84]  Cathy J. Price,et al.  Structural Correlates of Semantic and Phonemic Fluency Ability in First and Second Languages , 2009, Cerebral cortex.

[85]  Cornelius Weiller,et al.  Revisiting the Functional Specialization of Left Inferior Frontal Gyrus in Phonological and Semantic Fluency: The Crucial Role of Task Demands and Individual Ability , 2013, The Journal of Neuroscience.

[86]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[87]  S. Costafreda Parametric coordinate-based meta-analysis: Valid effect size meta-analysis of studies with differing statistical thresholds , 2012, Journal of Neuroscience Methods.

[88]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[89]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[90]  Sophie Schwartz,et al.  Role of frontal versus temporal cortex in verbal fluency as revealed by voxel-based lesion symptom mapping , 2006, Journal of the International Neuropsychological Society.

[91]  Sergi G. Costafreda,et al.  Pooling fMRI Data: Meta-Analysis, Mega-Analysis and Multi-Center Studies , 2009, Front. Neuroinform..

[92]  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.