A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus

The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation o...

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Published inHuman brain mapping Vol. 27; no. 10; pp. 799 - 810
Main Authors Costafreda, Sergi G., Fu, Cynthia H.Y., Lee, Lucy, Everitt, Brian, Brammer, Michael J., David, Anthony S.
Format Journal Article
LanguageEnglish
Published Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.10.2006
Wiley-Liss
Subjects
Online AccessGet full text
ISSN1065-9471
1097-0193
1097-0193
DOI10.1002/hbm.20221

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Abstract The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation of phonologic and semantic operations within the LIFG. An alternative theory proposes that both processes are encompassed within a supramodal executive function in a single region in the LIFG. To test these theories, we carried out a systematic review of functional magnetic resonance imaging studies employing phonologic and semantic verbal fluency tasks. Seventeen articles meeting our pre‐established criteria were found, consisting of 22 relevant experiments with 197 healthy subjects and a total of 41 peak activations in the LIFG. We determined 95% confidence intervals of the mean location (x, y, and z coordinates) of peaks of blood oxygenation level‐dependent (BOLD) responses from published phonologic and semantic verbal fluency studies using the nonparametric technique of bootstrap analysis. Significant differences were revealed in dorsal–ventral (z‐coordinate) localizations of the peak BOLD response: phonologic verbal fluency peak BOLD response was significantly more dorsal to the peak associated with semantic verbal fluency (confidence interval of difference: 1.9–17.4 mm). No significant differences were evident in antero–posterior (x‐coordinate) or medial–lateral (y‐coordinate) positions. The results support distinct dorsal–ventral locations for phonologic and semantic processes within the LIFG. Current limitations to meta‐analytic integration of published functional neuroimaging studies are discussed. Hum Brain Mapp, 2006. © 2006 Wiley‐Liss, Inc.
AbstractList The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation of phonologic and semantic operations within the LIFG. An alternative theory proposes that both processes are encompassed within a supramodal executive function in a single region in the LIFG. To test these theories, we carried out a systematic review of functional magnetic resonance imaging studies employing phonologic and semantic verbal fluency tasks. Seventeen articles meeting our pre-established criteria were found, consisting of 22 relevant experiments with 197 healthy subjects and a total of 41 peak activations in the LIFG. We determined 95% confidence intervals of the mean location (x, y, and z coordinates) of peaks of blood oxygenation level-dependent (BOLD) responses from published phonologic and semantic verbal fluency studies using the nonparametric technique of bootstrap analysis. Significant differences were revealed in dorsal-ventral (z-coordinate) localizations of the peak BOLD response: phonologic verbal fluency peak BOLD response was significantly more dorsal to the peak associated with semantic verbal fluency (confidence interval of difference: 1.9-17.4 mm). No significant differences were evident in antero-posterior (x-coordinate) or medial-lateral (y-coordinate) positions. The results support distinct dorsal-ventral locations for phonologic and semantic processes within the LIFG. Current limitations to meta-analytic integration of published functional neuroimaging studies are discussed.The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation of phonologic and semantic operations within the LIFG. An alternative theory proposes that both processes are encompassed within a supramodal executive function in a single region in the LIFG. To test these theories, we carried out a systematic review of functional magnetic resonance imaging studies employing phonologic and semantic verbal fluency tasks. Seventeen articles meeting our pre-established criteria were found, consisting of 22 relevant experiments with 197 healthy subjects and a total of 41 peak activations in the LIFG. We determined 95% confidence intervals of the mean location (x, y, and z coordinates) of peaks of blood oxygenation level-dependent (BOLD) responses from published phonologic and semantic verbal fluency studies using the nonparametric technique of bootstrap analysis. Significant differences were revealed in dorsal-ventral (z-coordinate) localizations of the peak BOLD response: phonologic verbal fluency peak BOLD response was significantly more dorsal to the peak associated with semantic verbal fluency (confidence interval of difference: 1.9-17.4 mm). No significant differences were evident in antero-posterior (x-coordinate) or medial-lateral (y-coordinate) positions. The results support distinct dorsal-ventral locations for phonologic and semantic processes within the LIFG. Current limitations to meta-analytic integration of published functional neuroimaging studies are discussed.
The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation of phonologic and semantic operations within the LIFG. An alternative theory proposes that both processes are encompassed within a supramodal executive function in a single region in the LIFG. To test these theories, we carried out a systematic review of functional magnetic resonance imaging studies employing phonologic and semantic verbal fluency tasks. Seventeen articles meeting our pre‐established criteria were found, consisting of 22 relevant experiments with 197 healthy subjects and a total of 41 peak activations in the LIFG. We determined 95% confidence intervals of the mean location (x, y, and z coordinates) of peaks of blood oxygenation level‐dependent (BOLD) responses from published phonologic and semantic verbal fluency studies using the nonparametric technique of bootstrap analysis. Significant differences were revealed in dorsal–ventral (z‐coordinate) localizations of the peak BOLD response: phonologic verbal fluency peak BOLD response was significantly more dorsal to the peak associated with semantic verbal fluency (confidence interval of difference: 1.9–17.4 mm). No significant differences were evident in antero–posterior (x‐coordinate) or medial–lateral (y‐coordinate) positions. The results support distinct dorsal–ventral locations for phonologic and semantic processes within the LIFG. Current limitations to meta‐analytic integration of published functional neuroimaging studies are discussed. Hum Brain Mapp, 2006. © 2006 Wiley‐Liss, Inc.
The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation of phonologic and semantic operations within the LIFG. An alternative theory proposes that both processes are encompassed within a supramodal executive function in a single region in the LIFG. To test these theories, we carried out a systematic review of functional magnetic resonance imaging studies employing phonologic and semantic verbal fluency tasks. Seventeen articles meeting our pre‐established criteria were found, consisting of 22 relevant experiments with 197 healthy subjects and a total of 41 peak activations in the LIFG. We determined 95% confidence intervals of the mean location ( x , y , and z coordinates) of peaks of blood oxygenation level‐dependent (BOLD) responses from published phonologic and semantic verbal fluency studies using the nonparametric technique of bootstrap analysis. Significant differences were revealed in dorsal–ventral ( z ‐coordinate) localizations of the peak BOLD response: phonologic verbal fluency peak BOLD response was significantly more dorsal to the peak associated with semantic verbal fluency (confidence interval of difference: 1.9–17.4 mm). No significant differences were evident in antero–posterior ( x ‐coordinate) or medial–lateral ( y ‐coordinate) positions. The results support distinct dorsal–ventral locations for phonologic and semantic processes within the LIFG. Current limitations to meta‐analytic integration of published functional neuroimaging studies are discussed. Hum Brain Mapp, 2006. © 2006 Wiley‐Liss, Inc.
The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation of phonologic and semantic operations within the LIFG. An alternative theory proposes that both processes are encompassed within a supramodal executive function in a single region in the LIFG. To test these theories, we carried out a systematic review of functional magnetic resonance imaging studies employing phonologic and semantic verbal fluency tasks. Seventeen articles meeting our pre-established criteria were found, consisting of 22 relevant experiments with 197 healthy subjects and a total of 41 peak activations in the LIFG. We determined 95% confidence intervals of the mean location (x, y, and z coordinates) of peaks of blood oxygenation level-dependent (BOLD) responses from published phonologic and semantic verbal fluency studies using the nonparametric technique of bootstrap analysis. Significant differences were revealed in dorsal-ventral (z-coordinate) localizations of the peak BOLD response: phonologic verbal fluency peak BOLD response was significantly more dorsal to the peak associated with semantic verbal fluency (confidence interval of difference: 1.9-17.4 mm). No significant differences were evident in antero-posterior (x-coordinate) or medial-lateral (y-coordinate) positions. The results support distinct dorsal-ventral locations for phonologic and semantic processes within the LIFG. Current limitations to meta-analytic integration of published functional neuroimaging studies are discussed. Hum Brain Mapp, 2006.
The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two main theories have proposed a different functional organization in the LIFG for these processes. One theory suggests an anatomic parcellation of phonologic and semantic operations within the LIFG. An alternative theory proposes that both processes are encompassed within a supramodal executive function in a single region in the LIFG. To test these theories, we carried out a systematic review of functional magnetic resonance imaging studies employing phonologic and semantic verbal fluency tasks. Seventeen articles meeting our pre-established criteria were found, consisting of 22 relevant experiments with 197 healthy subjects and a total of 41 peak activations in the LIFG. We determined 95% confidence intervals of the mean location (x, y, and z coordinates) of peaks of blood oxygenation level-dependent (BOLD) responses from published phonologic and semantic verbal fluency studies using the nonparametric technique of bootstrap analysis. Significant differences were revealed in dorsal-ventral (z-coordinate) localizations of the peak BOLD response: phonologic verbal fluency peak BOLD response was significantly more dorsal to the peak associated with semantic verbal fluency (confidence interval of difference: 1.9-17.4 mm). No significant differences were evident in antero-posterior (x-coordinate) or medial-lateral (y-coordinate) positions. The results support distinct dorsal-ventral locations for phonologic and semantic processes within the LIFG. Current limitations to meta-analytic integration of published functional neuroimaging studies are discussed.
Author Costafreda, Sergi G.
Brammer, Michael J.
David, Anthony S.
Lee, Lucy
Fu, Cynthia H.Y.
Everitt, Brian
AuthorAffiliation 1 Brain Image Analysis Unit, Department of Biostatistics and Computing, Institute of Psychiatry, King's College London, London, United Kingdom
4 Functional Imaging Laboratory, Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, London, United Kingdom
2 Division of Psychological Medicine, Institute of Psychiatry, King's College London, London, United Kingdom
3 Social, Genetic, and Developmental Psychiatry Centre, Institute of Psychiatry, King's College London, London, United Kingdom
AuthorAffiliation_xml – name: 1 Brain Image Analysis Unit, Department of Biostatistics and Computing, Institute of Psychiatry, King's College London, London, United Kingdom
– name: 2 Division of Psychological Medicine, Institute of Psychiatry, King's College London, London, United Kingdom
– name: 4 Functional Imaging Laboratory, Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, London, United Kingdom
– name: 3 Social, Genetic, and Developmental Psychiatry Centre, Institute of Psychiatry, King's College London, London, United Kingdom
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  givenname: Sergi G.
  surname: Costafreda
  fullname: Costafreda, Sergi G.
  email: s.costafreda@iop.kcl.ac.uk
  organization: Brain Image Analysis Unit, Department of Biostatistics and Computing, Institute of Psychiatry, King's College London, London, United Kingdom
– sequence: 2
  givenname: Cynthia H.Y.
  surname: Fu
  fullname: Fu, Cynthia H.Y.
  organization: Division of Psychological Medicine, Institute of Psychiatry, King's College London, London, United Kingdom
– sequence: 3
  givenname: Lucy
  surname: Lee
  fullname: Lee, Lucy
  organization: Functional Imaging Laboratory, Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, London, United Kingdom
– sequence: 4
  givenname: Brian
  surname: Everitt
  fullname: Everitt, Brian
  organization: Brain Image Analysis Unit, Department of Biostatistics and Computing, Institute of Psychiatry, King's College London, London, United Kingdom
– sequence: 5
  givenname: Michael J.
  surname: Brammer
  fullname: Brammer, Michael J.
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– sequence: 6
  givenname: Anthony S.
  surname: David
  fullname: David, Anthony S.
  organization: Division of Psychological Medicine, Institute of Psychiatry, King's College London, London, United Kingdom
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Frontal cortex
Prefrontal cortex
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Encephalon
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Frontal
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References Fox PT, Huang AY, Parsons LW, Xiong JH, Rainey L, Lancaster JL (1999): Functional volumes modeling: scaling for group size in averaged images. Hum Brain Mapp 8: 143-150.
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Brammer MJ, Bullmore ET, Simmons A, Williams SC, Grasby PM, Howard RJ, Woodruff PW, Rabe-Hesketh S (1997): Generic brain activation mapping in functional magnetic resonance imaging: a non-parametric approach. Magn Reson Imaging 15: 763-770.
Manly BF (1997): Randomization, bootstrapping and Monte Carlo methods in biology (2nd ed.). Boca Raton, FL: Chapman and Hall/CRC. 424 p.
Brett M, Johnsrude IS, Owen AM (2002): The problem of functional localization in the human brain. Nat Rev Neurosci 3: 243-249.
Gold BT, Buckner RL (2002): Common prefrontal regions coactivate with dissociable posterior regions during controlled semantic and phonological tasks. Neuron 35: 8030 -812.
McDermott KB, Petersen SE, Watson JM, Ojemann JG (2003): A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging. Neuropsychologia 41: 293 -303.
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Snippet The left inferior frontal gyrus (LIFG) has consistently been associated with both phonologic and semantic operations in functional neuroimaging studies. Two...
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SubjectTerms Biological and medical sciences
Brain Mapping
data pooling
Electrodiagnosis. Electric activity recording
Frontal Lobe - physiology
functional magnetic resonance imaging
Fundamental and applied biological sciences. Psychology
Human
Humans
inferior frontal cortex
Investigative techniques, diagnostic techniques (general aspects)
language
Learning. Memory
Magnetic Resonance Imaging
Medical sciences
Memory
meta-analysis
Nervous system
nonparametric statistics
prefrontal cortex
Psychology. Psychoanalysis. Psychiatry
Psychology. Psychophysiology
Radiodiagnosis. Nmr imagery. Nmr spectrometry
Verbal Behavior - physiology
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Title A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal gyrus
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