Functional organization of the left inferior precentral sulcus: Dissociating the inferior frontal eye field and the inferior frontal junction

Two eye fields have been described in the human lateral frontal cortex: the frontal eye field (FEF) and the inferior frontal eye field (iFEF). The FEF has been extensively studied and has been found to lie at the ventral part of the superior precentral sulcus. Much less research, however, has focused on the iFEF. Recently, it was suggested that the iFEF is located at the dorsal part of the inferior precentral sulcus. A similar location was proposed for the inferior frontal junction area (IFJ), an area thought to be involved in cognitive control processes. The present study used fMRI to clarify the topographical and functional relationship of the iFEF and the IFJ in the left hemispheres of individual participants. The results show that both the iFEF and the IFJ are indeed located at the dorsal part of the inferior precentral sulcus. Nevertheless, the activations were spatially dissociable in every individual examined. The IFJ was located more towards the depth of the inferior precentral sulcus, close to the junction with the inferior frontal sulcus, whereas the iFEF assumed a more lateral, posterior and superior position. Furthermore, the results provided evidence for a functional double dissociation: the iFEF was activated only in a comparison of saccades vs. button presses, but not in a comparison of incongruent vs. congruent Stroop conditions, while the opposite pattern was found at the IFJ. These results provide evidence for a spatial and functional dissociation of two directly adjacent areas in the left posterior frontal lobe.

[1]  R. J. Seitz,et al.  Activation of frontoparietal cortices during memorized triple‐step sequences of saccadic eye movements: an fMRI study , 2001, The European journal of neuroscience.

[2]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[3]  Michael Petrides,et al.  Local Morphology Predicts Functional Organization of the Dorsal Premotor Region in the Human Brain , 2006, The Journal of Neuroscience.

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

[5]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[6]  J Tanji,et al.  An oculomotor representation area within the ventral premotor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  C. Michel,et al.  PET study of human voluntary saccadic eye movements in darkness: effect of task repetition on the activation pattern , 1998, The European journal of neuroscience.

[8]  Stephen M. Smith,et al.  Functional MRI : an introduction to methods , 2002 .

[9]  E. Wagenmakers.  A practical solution to the pervasive problems ofp values , 2007, Psychonomic bulletin & review.

[10]  Michael Petrides,et al.  Anatomical organization of the eye fields in the human and non-human primate frontal cortex , 2009, Progress in Neurobiology.

[11]  Roger B. H. Tootell,et al.  Does Retinotopy Influence Cortical Folding in Primate Visual Cortex? , 2009, The Journal of Neuroscience.

[12]  M. Brass,et al.  Neural activations at the junction of the inferior frontal sulcus and the inferior precentral sulcus: Interindividual variability, reliability, and association with sulcal morphology , 2009, Human brain mapping.

[13]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[14]  H. Collewijn,et al.  Human eye movements associated with blinks and prolonged eyelid closure. , 1985, Journal of neurophysiology.

[15]  Makoto Kato,et al.  Functional MRI of brain activation evoked by intentional eye blinking , 2003, NeuroImage.

[16]  A. Berthoz,et al.  Functional Anatomy of a Prelearned Sequence of Horizontal Saccades in Humans , 1996, The Journal of Neuroscience.

[17]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[18]  Gabriele Lohmann,et al.  Magnetic resonance imaging of the human frontal cortex reveals differential anterior–posterior variability of sulcal basins , 2005, NeuroImage.

[19]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[20]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[21]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[22]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[23]  R W Cox,et al.  Software tools for analysis and visualization of fMRI data , 1997, NMR in biomedicine.

[24]  M. Corbetta,et al.  Frontoparietal Cortex Controls Spatial Attention through Modulation of Anticipatory Alpha Rhythms , 2009, The Journal of Neuroscience.

[25]  D. Norris,et al.  BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: Parallel‐acquired inhomogeneity‐desensitized fMRI , 2006, Magnetic resonance in medicine.

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

[27]  Oscar. Eberstaller,et al.  Das Stirnhirn : ein Beitrag zur Anatomie der Oberfläche des Grosshirns , 1890 .

[28]  L. Bour,et al.  Neurophysiological aspects of eye and eyelid movements during blinking in humans. , 2000, Journal of neurophysiology.

[29]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[30]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[31]  Theodore P. Zanto,et al.  Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory , 2011, Nature Neuroscience.

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

[33]  Makoto Kato,et al.  Human precentral cortical activation patterns during saccade tasks: an fMRI comparison with activation during intentional eyeblink tasks , 2003, NeuroImage.

[34]  Michael S. Beauchamp,et al.  A new method for improving functional-to-structural MRI alignment using local Pearson correlation , 2009, NeuroImage.

[35]  A. Berthoz,et al.  Localization of human frontal eye fields: anatomical and functional findings of functional magnetic resonance imaging and intracerebral electrical stimulation. , 2001, Journal of neurosurgery.

[36]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[37]  M. Brass,et al.  The role of the frontal cortex in task preparation. , 2002, Cerebral cortex.

[38]  P. Goldman-Rakic,et al.  Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach Coordinate System. , 1995, Cerebral cortex.

[39]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[40]  M. Brass,et al.  The role of the inferior frontal junction area in cognitive control , 2005, Trends in Cognitive Sciences.

[41]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[42]  Alexander Ecker.  Die Hirnwindungen des Menschen nach eigenen Untersuchungen : insbesondere über die Entwicklung derselben beim Fötus und mit Rücksicht auf das Bedürfniss der Ärzte , 1869 .

[43]  Christopher Kennard,et al.  Differential cortical activation during voluntary and reflexive saccades in man , 2003, NeuroImage.

[44]  M. Brass,et al.  Involvement of the inferior frontal junction in cognitive control: Meta‐analyses of switching and Stroop studies , 2005, Human brain mapping.

[45]  Michael Petrides,et al.  Precentral sulcal complex of the human brain: Morphology and statistical probability maps , 2005, The Journal of comparative neurology.

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

[47]  Wilder Penfield,et al.  THE CEREBRAL CORTEX IN MAN: I. THE CEREBRAL CORTEX AND CONSCIOUSNESS , 1938 .

[48]  Jan Derrfuss,et al.  Cognitive control in the posterior frontolateral cortex: evidence from common activations in task coordination, interference control, and working memory , 2004, NeuroImage.

[49]  Keith J. Worsley,et al.  Statistical analysis of activation images , 2001 .

[50]  Lawrence L. Wald,et al.  Accurate prediction of V1 location from cortical folds in a surface coordinate system , 2008, NeuroImage.

[51]  A. Aron,et al.  Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex , 2010, Proceedings of the National Academy of Sciences.

[52]  O. Blanke,et al.  Location of the human frontal eye field as defined by electrical cortical stimulation: anatomical, functional and electrophysiological characteristics , 2000, Neuroreport.

[53]  O. Vogt,et al.  Die vergleichend-architektonische und die vergleichend-reizphysiologische Felderung der Großhirnrinde unter besonderer Berücksichtigung der menschlichen , 1926, Naturwissenschaften.

[54]  山浦 晶.  Atlas of the Cerebral Sulci, Michio Ono, Stefan Kubik and Chad D. Abernathey著, Georg Thieme Verlag, Stuttgart, New York 1990(らいぶらりい) , 1992 .

[55]  C. Svarer,et al.  Parieto-occipital cortex activation during self-generated eye movements in the dark. , 1998, Brain : a journal of neurology.

[56]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[57]  Nancy Kanwisher,et al.  Neuroimaging of Language: Why Hasn't a Clearer Picture Emerged? , 2009, Lang. Linguistics Compass.

[58]  M. Brass,et al.  Decomposing Components of Task Preparation with Functional Magnetic Resonance Imaging , 2004, Journal of Cognitive Neuroscience.

[59]  Claus C. Hilgetag,et al.  Role of Mechanical Factors in the Morphology of the Primate Cerebral Cortex , 2006, PLoS Comput. Biol..

[60]  C R Genovese,et al.  Cortical networks subserving pursuit and saccadic eye movements in humans: An FMRI study , 1999, Human brain mapping.

[61]  Adam Gazzaley,et al.  Top-down modulation of visual feature processing: The role of the inferior frontal junction , 2010, NeuroImage.

[62]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[63]  Hiroki M. Morimoto,et al.  Functional dissociation in right inferior frontal cortex during performance of go/no-go task. , 2009, Cerebral cortex.

[64]  M. Masson.  Using confidence intervals for graphically based data interpretation. , 2003, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[65]  B. J. McCurtain,et al.  Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study. , 1998, Cerebral cortex.