Connectivity-based subdivisions of the human right "temporoparietal junction area": evidence for different areas participating in different cortical networks.

Controversy surrounds the role of the temporoparietal junction (TPJ) area of the human brain. Although TPJ has been implicated both in reorienting of attention and social cognition, it is still unclear whether these functions have the same neural basis. Indeed, whether TPJ is a precisely identifiable cortical region or a cluster of subregions with separate functions is still a matter of debate. Here, we examined the structural and functional connectivity of TPJ, testing whether TPJ is a unitary area with a heterogeneous functional connectivity profile or a conglomerate of regions with distinctive connectivity. Diffusion-weighted imaging tractrography-based parcellation identified 3 separate regions in TPJ. Resting-state functional connectivity was then used to establish which cortical networks each of these subregions participates in. A dorsal cluster in the middle part of the inferior parietal lobule showed resting-state functional connectivity with, among other areas, lateral anterior prefrontal cortex. Ventrally, an anterior TPJ cluster interacted with ventral prefrontal cortex and anterior insula, while a posterior TPJ cluster interacted with posterior cingulate, temporal pole, and anterior medial prefrontal cortex. These results indicate that TPJ can be subdivided into subregions on the basis of its structural and functional connectivity.

[1]  James C. Bezdek,et al.  Pattern Recognition with Fuzzy Objective Function Algorithms , 1981, Advanced Applications in Pattern Recognition.

[2]  R. Knight,et al.  Contributions of temporal-parietal junction to the human auditory P3 , 1989, Brain Research.

[3]  S. Yamaguchi,et al.  Anterior and posterior association cortex contributions to the somatosensory P300 , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

[6]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[7]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[8]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[9]  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.

[10]  Klaas E. Stephan,et al.  The anatomical basis of functional localization in the cortex , 2002, Nature Reviews Neuroscience.

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

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

[13]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[14]  C. Kennard,et al.  The anatomy of visual neglect , 2003 .

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

[16]  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.

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

[18]  Hanneke E. M. den Ouden,et al.  Thinking about intentions , 2005, NeuroImage.

[19]  R. Saxe,et al.  Making sense of another mind: The role of the right temporo-parietal junction , 2005, Neuropsychologia.

[20]  Stanislas Dehaene,et al.  From monkey brain to human brain : a Fyssen Foundation symposium , 2005 .

[21]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[22]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[23]  J. Decety,et al.  The power of simulation: Imagining one's own and other's behavior , 2006, Brain Research.

[24]  R. Sparing,et al.  Hemiextinction induced by transcranial magnetic stimulation over the right temporo-parietal junction , 2006, Neuroscience.

[25]  Michael Erb,et al.  Exploring the visual world: The neural substrate of spatial orienting , 2006, NeuroImage.

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

[27]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[28]  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.

[29]  R. Saxe.  Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

[30]  C. Frith,et al.  The Neural Basis of Mentalizing , 2006, Neuron.

[31]  Maurizio Corbetta,et al.  Visuospatial reorienting signals in the human temporo‐parietal junction are independent of response selection , 2006, The European journal of neuroscience.

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

[33]  Desmond J. Higham,et al.  Connectivity-based parcellation of human cortex using diffusion MRI: Establishing reproducibility, validity and observer independence in BA 44/45 and SMA/pre-SMA , 2007, NeuroImage.

[34]  D. V. Essen,et al.  Surface-Based and Probabilistic Atlases of Primate Cerebral Cortex , 2007, Neuron.

[35]  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.

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

[37]  J. Decety,et al.  The Role of the Right Temporoparietal Junction in Social Interaction: How Low-Level Computational Processes Contribute to Meta-Cognition , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[39]  Richard E. Passingham,et al.  What is special about the human brain , 2008 .

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

[41]  Manos Tsakiris,et al.  The role of the right temporo-parietal junction in maintaining a coherent sense of one's body , 2008, Neuropsychologia.

[42]  Peter Bossaerts,et al.  Neural correlates of mentalizing-related computations during strategic interactions in humans , 2008, Proceedings of the National Academy of Sciences.

[43]  Mark W Woolrich,et al.  Associative learning of social value , 2008, Nature.

[44]  S. Debener,et al.  Trial-by-Trial Fluctuations in the Event-Related Electroencephalogram Reflect Dynamic Changes in the Degree of Surprise , 2008, The Journal of Neuroscience.

[45]  Mark W. Woolrich,et al.  Robust group analysis using outlier inference , 2008, NeuroImage.

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

[47]  Jason P. Mitchell.  Activity in right temporo-parietal junction is not selective for theory-of-mind. , 2008, Cerebral cortex.

[48]  B. Averbeck,et al.  The primate cortical auditory system and neural representation of conspecific vocalizations. , 2009, Annual review of neuroscience.

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

[50]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

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

[52]  R. Mars,et al.  Comparing Brain Connections in Different Species using Diffusion Weighted Imaging , 2009 .

[53]  Emery N. Brown,et al.  Distinct Regions of Right Temporo-Parietal Junction Are Selective for Theory of Mind and Exogenous Attention , 2009, PloS one.

[54]  Sarah-Jayne Blakemore,et al.  Functional connectivity during a social emotion task in adolescents and in adults , 2009, The European journal of neuroscience.

[55]  M. Rushworth,et al.  General Mechanisms for Making Decisions? This Review Comes from a Themed Issue on Cognitive Neuroscience Edited the Representation of Value and Reward Expectations in Frontal Cortex Reward Prediction Errors and Learning Rates Other Types of Prediction Error , 2022 .

[56]  T. Metzinger,et al.  Full-body illusions and minimal phenomenal selfhood , 2009, Trends in Cognitive Sciences.

[57]  T. Singer,et al.  The role of anterior insular cortex in social emotions , 2010, Brain Structure and Function.

[58]  Itamar Kahn,et al.  Functional connectivity of the macaque posterior parahippocampal cortex. , 2010, Journal of neurophysiology.

[59]  H. Johansen-Berg,et al.  Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. , 2010, Cerebral cortex.

[60]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[61]  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.