Revisiting the Functional Specialization of Left Inferior Frontal Gyrus in Phonological and Semantic Fluency: The Crucial Role of Task Demands and Individual Ability

Despite a large body of research, extant findings on the functional role of left inferior frontal gyrus (LIFG) in phonological and semantic fluency are still controversial. Based on cross-study comparisons, a recent meta-analysis of neuroimaging results suggests that posterior-dorsal (Brodmann area, BA, 44) and anterior-ventral parts (BA 45) of LIFG contribute differentially to processes of phonologically and semantically cued word retrieval, respectively. In contrast, a subsequent functional magnetic resonance imaging experiment failed to validate the proposed dissociation using a within-subjects design. In particular, no evidence for a specific role of BA 45 in semantic fluency was found. Here, we resolve this apparent controversy by showing that the conflicting findings can be accounted for when considering the influence of task demands and individual ability on resulting functional magnetic resonance imaging activation patterns. By comparing phonological versus semantic fluency, higher activation was robustly observed in BA 44. For the opposite comparison, higher activation was found in dorsal BA 45; however, this was more pronounced in posterior-dorsal parts of BA 45 for low-performing subjects and was only apparent in anterior-dorsal parts of BA 45 under high demands on controlled semantic retrieval. Our results thus disclose important determinants for detecting a functional segregation of LIFG in verbal fluency that also have implications for the controversial findings in previous lesion studies. Moreover, the present parcellation of dorsal BA 45 corresponds well with anatomical evidence suggesting a subdivision into an anterior (45A) and posterior part (45B) and may therefore represent evidence for its functional significance in humans.

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

[2]  Gene A. Brewer,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology Variation in Verbal Fluency: a Latent Variable Analysis of Clustering, Switching, and Overall Performance , 2022 .

[3]  Tamiko Azuma,et al.  Working memory and perseveration in verbal fluency. , 2004, Neuropsychology.

[4]  L. Cipolotti,et al.  Dynamic aphasia: an inability to select between competing verbal responses? , 1998, Brain : a journal of neurology.

[5]  G. Luppino,et al.  Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. , 2010, Cerebral cortex.

[6]  G. Winocur,et al.  Clustering and switching as two components of verbal fluency: evidence from younger and older healthy adults. , 1997, Neuropsychology.

[7]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[8]  E. Capitani,et al.  Qualitative features of semantic fluency performance in mesial and lateral frontal patients , 2006, Neuropsychologia.

[9]  P. Morosan,et al.  Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping , 2010, PLoS biology.

[10]  Peter Brugger,et al.  Pervasive influence of semantics in letter and category fluency: A multidimensional approach , 2003, Brain and Language.

[11]  G. Luppino,et al.  Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey , 2007, Brain Structure and Function.

[12]  W. Sturm,et al.  Neuropsychological assessment , 2007, Journal of Neurology.

[13]  E. Perret The left frontal lobe of man and the suppression of habitual responses in verbal categorical behaviour. , 1974, Neuropsychologia.

[14]  Simon B. Eickhoff,et al.  Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps , 2006, NeuroImage.

[15]  D. Perani,et al.  Functional heterogeneity of left inferior frontal cortex as revealed by fMRI , 1997, Neuroreport.

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

[17]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[18]  Willem J. M. Levelt,et al.  The neural correlates of language production , 2000 .

[19]  M Zaitsev,et al.  Point spread function mapping with parallel imaging techniques and high acceleration factors: Fast, robust, and flexible method for echo‐planar imaging distortion correction , 2004, Magnetic resonance in medicine.

[20]  Irene P. Kan,et al.  Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  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.

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

[23]  Gail Ramsberger,et al.  Commonalities and differences in the working memory components underlying letter and category fluency tasks: a dual-task investigation. , 2002, Neuropsychology.

[24]  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.

[25]  P. Lachenbruch Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[26]  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.

[27]  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.

[28]  J. Hodges,et al.  Generating ‘tiger’ as an animal name or a word beginning with T: differences in brain activation , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  G. Lockhead,et al.  The free recall of category examples. , 1980 .

[30]  Marco Bozzali,et al.  The differing roles of the frontal cortex in fluency tests. , 2012, Brain : a journal of neurology.

[31]  O. Selnes A Compendium of Neuropsychological Tests , 1991, Neurology.

[32]  D. Pandya,et al.  Distinct Parietal and Temporal Pathways to the Homologues of Broca's Area in the Monkey , 2009, PLoS biology.

[33]  R. Engle,et al.  The role of working memory capacity in retrieval. , 1997, Journal of experimental psychology. General.

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

[35]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[36]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[37]  R. Kliegl,et al.  Complex semantic processing in old age: does it stay or does it go? , 2000, Psychology and aging.

[38]  G. Winocur,et al.  Clustering and switching on verbal fluency: the effects of focal frontal- and temporal-lobe lesions , 1998, Neuropsychologia.

[39]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[40]  J D Van Horn,et al.  A comparison of rCBF patterns during letter and semantic fluency. , 2000, Neuropsychology.

[41]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[42]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

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

[44]  D. Stuss,et al.  The effects of focal anterior and posterior brain lesions on verbal fluency , 1998, Journal of the International Neuropsychological Society.

[45]  Arthur L. Benton,et al.  Differential behavioral effects in frontal lobe disease , 1968 .

[46]  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.

[47]  G. Luppino,et al.  Thalamic projections to the macaque caudal ventrolateral prefrontal areas 45A and 45B , 2010, The European journal of neuroscience.

[48]  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.

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

[50]  J. Henry,et al.  A meta-analytic review of verbal fluency performance following focal cortical lesions. , 2004, Neuropsychology.

[51]  Alfred Anwander,et al.  Segregating the core computational faculty of human language from working memory , 2009, Proceedings of the National Academy of Sciences.

[52]  K. Boone,et al.  Handbook of Normative Data for Neuropsychological Assessment , 1999 .

[53]  Allan Collins,et al.  A spreading-activation theory of semantic processing , 1975 .

[54]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.