Functional topography of the right inferior parietal lobule structured by anatomical connectivity profiles

The nature of the relationship between structure and function is a fundamental question in neuroscience, especially at the macroscopic neuroimaging level. Although mounting studies have revealed that functional connectivity reflects structural connectivity, whether similar structural and functional connectivity patterns can reveal corresponding similarities in the structural and functional topography remains an open problem. In our current study, we used the right inferior parietal lobule (RIPL), which has been demonstrated to have similar anatomical and functional connectivity patterns at the subregional level, to directly test the hypothesis that similar structural and functional connectivity patterns can inform the corresponding topography of this area. In addition, since the association between the RIPL regions and particular functions and networks is still largely unknown, post‐hoc functional characterizations and connectivity analyses were performed to identify the main functions and cortical networks in which each subregion participated. Anatomical and functional connectivity‐based parcellations of the RIPL have consistently identified five subregions. Our functional characterization using meta‐analysis‐based behavioral and connectivity analyses revealed that the two anterior subregions (Cl1 and Cl2) primarily participate in interoception and execution, respectively; whereas the posterior subregion (Cl3) in the SMG primarily participates in attention and action inhibition. The two posterior subregions (Cl4, Cl5) in the AG were primarily involved in social cognition and spatial cognition, respectively. These results indicated that similar anatomical and functional connectivity patterns of the RIPL are reflected in corresponding structural and functional topographies. The identified cortical connectivity and functional characterization of each subregion may facilitate RIPL‐related clinical research. Hum Brain Mapp 37:4316–4332, 2016. © 2016 Wiley Periodicals, Inc.

[1]  Tianzi Jiang,et al.  The Neuroanatomical Basis for Posterior Superior Parietal Lobule Control Lateralization of Visuospatial Attention , 2016, Front. Neuroanat..

[2]  Tianzi Jiang,et al.  Determination of the posterior boundary of Wernicke's area based on multimodal connectivity profiles , 2015, Human brain mapping.

[3]  Tianzi Jiang,et al.  Convergent functional architecture of the superior parietal lobule unraveled with multimodal neuroimaging approaches , 2015, Human brain mapping.

[4]  Tianzi Jiang,et al.  Connectivity-based parcellation of the human temporal pole using diffusion tensor imaging. , 2014, Cerebral cortex.

[5]  Robert Turner,et al.  Connectivity architecture and subdivision of the human inferior parietal cortex revealed by diffusion MRI. , 2014, Cerebral cortex.

[6]  Ravi S. Menon,et al.  Identification of Optimal Structural Connectivity Using Functional Connectivity and Neural Modeling , 2014, The Journal of Neuroscience.

[7]  Chunshui Yu,et al.  Connectivity-based parcellation of the human posteromedial cortex. , 2014, Cerebral Cortex.

[8]  Adam G. Thomas,et al.  Comparison of Human Ventral Frontal Cortex Areas for Cognitive Control and Language with Areas in Monkey Frontal Cortex , 2014, Neuron.

[9]  Mary Beth Nebel,et al.  Disruption of functional organization within the primary motor cortex in children with autism , 2014, Human brain mapping.

[10]  Angela R. Laird,et al.  Tackling the multifunctional nature of Broca's region meta-analytically: Co-activation-based parcellation of area 44 , 2013, NeuroImage.

[11]  Angela R. Laird,et al.  Networks of task co-activations , 2013, NeuroImage.

[12]  Wei Li,et al.  Subregions of the human superior frontal gyrus and their connections , 2013, NeuroImage.

[13]  Alex Martin,et al.  Two distinct forms of functional lateralization in the human brain , 2013, Proceedings of the National Academy of Sciences.

[14]  Hang Joon Jo,et al.  Correcting Brain-Wide Correlation Differences in Resting-State FMRI , 2013, Brain Connect..

[15]  Adam G. Thomas,et al.  The Organization of Dorsal Frontal Cortex in Humans and Macaques , 2013, The Journal of Neuroscience.

[16]  Hang Joon Jo,et al.  The perils of global signal regression for group comparisons: a case study of Autism Spectrum Disorders , 2013, Front. Hum. Neurosci..

[17]  Maurizio Corbetta,et al.  Resting-State Functional Connectivity Emerges from Structurally and Dynamically Shaped Slow Linear Fluctuations , 2013, The Journal of Neuroscience.

[18]  Chunshui Yu,et al.  Connectivity-Based Parcellation of the Human Frontal Pole with Diffusion Tensor Imaging , 2013, The Journal of Neuroscience.

[19]  Angela R. Laird,et al.  Is There “One” DLPFC in Cognitive Action Control? Evidence for Heterogeneity From Co-Activation-Based Parcellation , 2012, Cerebral cortex.

[20]  K. Zilles,et al.  An investigation of the structural, connectional, and functional subspecialization in the human amygdala , 2012, Human brain mapping.

[21]  A. Schleicher,et al.  Organization of the Human Inferior Parietal Lobule Based on Receptor Architectonics , 2012, Cerebral cortex.

[22]  K. Zilles,et al.  Differentiated parietal connectivity of frontal regions for “what” and “where” memory , 2012, Brain Structure and Function.

[23]  Yu Zhang,et al.  Tractography‐based parcellation of the human left inferior parietal lobule , 2012, NeuroImage.

[24]  M. Rushworth,et al.  Connectivity-based subdivisions of the human right "temporoparietal junction area": evidence for different areas participating in different cortical networks. , 2012, Cerebral cortex.

[25]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[26]  Michael P. Milham,et al.  A convergent functional architecture of the insula emerges across imaging modalities , 2012, NeuroImage.

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

[28]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[29]  M. Catani,et al.  A lateralized brain network for visuospatial attention , 2011, Nature Neuroscience.

[30]  Nadim Joni Shah,et al.  Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques , 2011, NeuroImage.

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

[32]  S. Eickhoff,et al.  Approaches for the Integrated Analysis of Structure, Function and Connectivity of the Human Brain , 2011, Clinical EEG and neuroscience.

[33]  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.

[34]  R. Mar The neural bases of social cognition and story comprehension. , 2011, Annual review of psychology.

[35]  Kaustubh Supekar,et al.  Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. , 2010, Cerebral cortex.

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

[37]  M. Fox,et al.  Noninvasive functional and structural connectivity mapping of the human thalamocortical system. , 2010, Cerebral cortex.

[38]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[39]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[40]  Sang Won Seo,et al.  Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: Functional connectivity-based parcellation method , 2010, NeuroImage.

[41]  William W. Graves,et al.  Neural Systems for Reading Aloud: A Multiparametric Approach , 2009, Cerebral cortex.

[42]  P. Fox,et al.  Metaanalytic connectivity modeling: Delineating the functional connectivity of the human amygdala , 2009, Human brain mapping.

[43]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[44]  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.

[45]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[46]  Timothy Edward John Behrens,et al.  How Green Is the Grass on the Other Side? Frontopolar Cortex and the Evidence in Favor of Alternative Courses of Action , 2009, Neuron.

[47]  Glyn W. Humphreys,et al.  Reflexive and Preparatory Selection and Suppression of Salient Information in the Right and Left Posterior Parietal Cortex , 2009, Journal of Cognitive Neuroscience.

[48]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[49]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[50]  Catie Chang,et al.  Influence of heart rate on the BOLD signal: The cardiac response function , 2009, NeuroImage.

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

[52]  D. Pandya,et al.  The extreme capsule in humans and rethinking of the language circuitry , 2009, Brain Structure and Function.

[53]  Vince D. Calhoun,et al.  Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations , 2008, NeuroImage.

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

[55]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[56]  Damien A. Fair,et al.  Defining functional areas in individual human brains using resting functional connectivity MRI , 2008, NeuroImage.

[57]  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.

[58]  J. Jonides,et al.  Interference resolution: Insights from a meta-analysis of neuroimaging tasks , 2007, Cognitive, affective & behavioral neuroscience.

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

[60]  A. Anwander,et al.  Connectivity-Based Parcellation of Broca's Area. , 2006, Cerebral cortex.

[61]  Adrian Raine,et al.  Neural foundations to moral reasoning and antisocial behavior. , 2006, Social cognitive and affective neuroscience.

[62]  Michael Vesia,et al.  Hemispheric asymmetry in memory-guided pointing during single-pulse transcranial magnetic stimulation of human parietal cortex. , 2006, Journal of neurophysiology.

[63]  Katrin Amunts,et al.  The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability , 2006, NeuroImage.

[64]  Gereon R. Fink,et al.  Cue validity modulates the neural correlates of covert endogenous orienting of attention in parietal and frontal cortex , 2006, NeuroImage.

[65]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[66]  G. Rizzolatti The mirror neuron system and its function in humans , 2005, Anatomy and Embryology.

[67]  Tor D. Wager,et al.  Common and unique components of response inhibition revealed by fMRI , 2005, NeuroImage.

[68]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[69]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

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

[71]  Scott T. Grafton,et al.  Cortical topography of human anterior intraparietal cortex active during visually guided grasping. , 2005, Brain research. Cognitive brain research.

[72]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[73]  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.

[74]  M. Weiner,et al.  Cognition and anatomy in three variants of primary progressive aphasia , 2004, Annals of neurology.

[75]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[76]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[77]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

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

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

[80]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[81]  David G. Norris,et al.  An Investigation of Functional and Anatomical Connectivity Using Magnetic Resonance Imaging , 2002, NeuroImage.

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

[83]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[84]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[85]  Barry D. Smith,et al.  Hemispheric asymmetry and emotion: Lateralized parietal processing of affect and cognition , 1987, Biological Psychology.

[86]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .