Subregions of the human superior frontal gyrus and their connections

The superior frontal gyrus (SFG) is located at the superior part of the prefrontal cortex and is involved in a variety of functions, suggesting the existence of functional subregions. However, parcellation schemes of the human SFG and the connection patterns of each subregion remain unclear. We firstly parcellated the human SFG into the anteromedial (SFGam), dorsolateral (SFGdl), and posterior (SFGp) subregions based on diffusion tensor tractography. The SFGam was anatomically connected with the anterior and mid-cingulate cortices, which are critical nodes of the cognitive control network and the default mode network (DMN). The SFGdl was connected with the middle and inferior frontal gyri, which are involved in the cognitive execution network. The SFGp was connected with the precentral gyrus, caudate, thalamus, and frontal operculum, which are nodes of the motor control network. Resting-state functional connectivity analysis further revealed that the SFGam was mainly correlated with the cognitive control network and the DMN; the SFGdl was correlated with the cognitive execution network and the DMN; and the SFGp was correlated with the sensorimotor-related brain regions. The SFGam and SFGdl were further parcellated into three and two subclusters that are well corresponding to Brodmann areas. These findings suggest that the human SFG consists of multiple dissociable subregions that have distinct connection patterns and that these subregions are involved in different functional networks and serve different functions. These results may improve our understanding on the functional complexity of the SFG and provide us an approach to investigate the SFG at the subregional level.

[1]  P. Morosan,et al.  Observer-Independent Method for Microstructural Parcellation of Cerebral Cortex: A Quantitative Approach to Cytoarchitectonics , 1999, NeuroImage.

[2]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

[3]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[4]  Morten L Kringelbach,et al.  Contrasting Connectivity of the Ventralis Intermedius and Ventralis Oralis Posterior Nuclei of the Motor Thalamus Demonstrated by Probabilistic Tractography , 2012, Neurosurgery.

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

[6]  Edward Awh,et al.  The anterior cingulate cortex lends a hand in response selection , 1999, Nature Neuroscience.

[7]  Masashi Kinoshita,et al.  Association fibers connecting the Broca center and the lateral superior frontal gyrus: a microsurgical and tractographic anatomy. , 2012, Journal of neurosurgery.

[8]  Mark V. Albert,et al.  Anticipation of conflict monitoring in the anterior cingulate cortex and the prefrontal cortex , 2007, Proceedings of the National Academy of Sciences.

[9]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[10]  B. Pfleiderer,et al.  Functional connectivity profile of the human inferior frontal junction: involvement in a cognitive control network , 2012, BMC Neuroscience.

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

[12]  B. Vogt,et al.  Human cingulate cortex: Surface features, flat maps, and cytoarchitecture , 1995, The Journal of comparative neurology.

[13]  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.

[14]  Karl J. Friston Functional integration and inference in the brain , 2002, Progress in Neurobiology.

[15]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[16]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[17]  Viviana Versace,et al.  Low frequency rTMS of the SMA transiently ameliorates peak-dose LID in Parkinson’s disease , 2006, Clinical Neurophysiology.

[18]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[19]  L. S. Boylana,et al.  Repetitive transcranial magnetic stimulation to SMA worsens complex movements in Parkinson ' s disease , 2001 .

[20]  W. Gehring,et al.  Functions of the Medial Frontal Cortex in the Processing of Conflict and Errors , 2001, The Journal of Neuroscience.

[21]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[22]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[23]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[24]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[25]  Simon B. Eickhoff,et al.  Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM , 2008, NeuroImage.

[26]  Wei Liao,et al.  Large-Scale Brain Networks in Board Game Experts: Insights from a Domain-Related Task and Task-Free Resting State , 2012, PloS one.

[27]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[28]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[29]  L. D. De Nil,et al.  Sequence skill learning in persons who stutter: implications for cortico-striato-thalamo-cortical dysfunction. , 2007, Journal of fluency disorders.

[30]  P. Goldman-Rakic,et al.  Prefrontal connections of medial motor areas in the rhesus monkey , 1993, The Journal of comparative neurology.

[31]  Carol A. Seger,et al.  How do the basal ganglia contribute to categorization? Their roles in generalization, response selection, and learning via feedback , 2008, Neuroscience & Biobehavioral Reviews.

[32]  Oliver Speck,et al.  Gender differences in the functional organization of the brain for working memory , 2000, Neuroreport.

[33]  W. G. Webster,et al.  Speech-Motor Control and Interhemispheric Relations in Recovered and Persistent Stuttering , 2001, Developmental neuropsychology.

[34]  Ming-Chyi Pai,et al.  Supplementary motor area aphasia: a case report , 1999, Clinical Neurology and Neurosurgery.

[35]  K. Amunts,et al.  The human inferior parietal lobule in stereotaxic space , 2008, Brain Structure and Function.

[36]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[37]  Lei Wang,et al.  Inter-rater reliability of manual segmentation of the superior, inferior and middle frontal gyri , 2006, Psychiatry Research: Neuroimaging.

[38]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[39]  Jie Wang,et al.  An Edge-Weighted Centroidal Voronoi Tessellation Model for Image Segmentation , 2009, IEEE Transactions on Image Processing.

[40]  Philippe A. Chouinard,et al.  Human Neuroscience , 2022 .

[41]  Gilles Pourtois,et al.  Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI , 2010, Neuropsychologia.

[42]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[43]  Yuan Zhou,et al.  Functional segregation of the human cingulate cortex is confirmed by functional connectivity based neuroanatomical parcellation , 2011, NeuroImage.

[44]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[45]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[46]  J. Pujol,et al.  Intrasurgical mapping of complex motor function in the superior frontal gyrus , 2011, Neuroscience.

[47]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[48]  M. Wiesendanger,et al.  The thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (macaca fascicularis) , 2004, Experimental Brain Research.

[49]  D. Sharp,et al.  Fractionating the Default Mode Network: Distinct Contributions of the Ventral and Dorsal Posterior Cingulate Cortex to Cognitive Control , 2011, The Journal of Neuroscience.

[50]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[51]  K. Amunts,et al.  Receptor mapping: architecture of the human cerebral cortex , 2009, Current opinion in neurology.

[52]  R. Passingham,et al.  The role of premotor and parietal cortex in the direction of action , 1982, Brain Research.

[53]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

[54]  Timothy Edward John Behrens,et al.  Anatomical and Functional Connectivity of Cytoarchitectonic Areas within the Human Parietal Operculum , 2010, The Journal of Neuroscience.

[55]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[56]  S. Carlson,et al.  Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. , 1998, Cerebral cortex.

[57]  Heidi Johansen-Berg,et al.  Using diffusion imaging to study human connectional anatomy. , 2009, Annual review of neuroscience.

[58]  Derek G. V. Mitchell,et al.  Common regions of dorsal anterior cingulate and prefrontal–parietal cortices provide attentional control of distracters varying in emotionality and visibility , 2007, NeuroImage.

[59]  Cameron S. Carter,et al.  Conflict-related activity in the caudal anterior cingulate cortex in the absence of awareness , 2009, Biological Psychology.

[60]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[61]  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..

[62]  M. Petrides Motor conditional associative-learning after selective prefrontal lesions in the monkey , 1982, Behavioural Brain Research.

[63]  K. Kawamura,et al.  Corticocortical projections to the prefrontal cortex in the rhesus monkey investigated with horseradish peroxidase techniques , 1984, Neuroscience Research.

[64]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Parietal Cortex and Comparison with Human and Macaque Resting-State Functional Connectivity , 2011, The Journal of Neuroscience.

[65]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[66]  U. Jürgens,et al.  The efferent and afferent connections of the supplementary motor area , 1984, Brain Research.

[67]  B. Dubois,et al.  Functions of the left superior frontal gyrus in humans: a lesion study. , 2006, Brain : a journal of neurology.

[68]  G. Northoff,et al.  Is Our Self Nothing but Reward? Neuronal Overlap and Distinction between Reward and Personal Relevance and Its Relation to Human Personality , 2009, PloS one.

[69]  K. Amunts,et al.  Centenary of Brodmann's Map — Conception and Fate , 2022 .

[70]  Francis Eustache,et al.  The Functional Neuroanatomy of Episodic Memory: The Role of the Frontal Lobes, the Hippocampal Formation, and Other Areas , 1998, NeuroImage.

[71]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[72]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[73]  Chaogan Yan,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010, Front. Syst. Neurosci..

[74]  Keith D. White,et al.  Structural connectivity of Broca's area and medial frontal cortex , 2010, NeuroImage.

[75]  Adrian M. Owen,et al.  The role of the lateral frontal cortex in mnemonic processing: the contribution of functional neuroimaging , 2000, Experimental Brain Research.

[76]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations , 2007, The Journal of Neuroscience.

[77]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[78]  M. Petrides,et al.  Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[79]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[80]  S E Petersen,et al.  Direct comparison of episodic encoding and retrieval of words: an event-related fMRI study. , 1999, Memory.

[81]  C. Frith,et al.  The functional neuroanatomy of episodic memory , 1997, Trends in Neurosciences.

[82]  Jae-Hong Lee,et al.  Stuttering and gait disturbance after supplementary motor area seizure , 2004, Movement disorders : official journal of the Movement Disorder Society.

[83]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[84]  R. Andersen,et al.  Posterior parietal cortex. , 1989, Reviews of oculomotor research.

[85]  Timothy Edward John Behrens,et al.  Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Robert Leech,et al.  Salience network integrity predicts default mode network function after traumatic brain injury , 2012, Proceedings of the National Academy of Sciences.

[87]  M. Petrides The role of the mid-dorsolateral prefrontal cortex in working memory , 2000, Experimental Brain Research.

[88]  Timothy E. J. Behrens,et al.  Deep and Superficial Amygdala Nuclei Projections Revealed In Vivo by Probabilistic Tractography , 2011, The Journal of Neuroscience.

[89]  Michelle Hampson,et al.  Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. , 2010, Magnetic resonance imaging.

[90]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[91]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[92]  Jun Tanji,et al.  Prefrontal cortical cells projecting to the supplementary eye field and presupplementary motor area in the monkey , 2005, Neuroscience Research.

[93]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[94]  Caterina Gratton,et al.  Double dissociation of two cognitive control networks in patients with focal brain lesions , 2010, Proceedings of the National Academy of Sciences.

[95]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.