Across-study and within-subject functional connectivity of a right temporo-parietal junction subregion involved in stimulus–context integration

Bidirectional integration between sensory stimuli and contextual framing is fundamental to action control. Stimuli may entail context-dependent actions, while temporal or spatial characteristics of a stimulus train may establish a contextual framework for upcoming stimuli. Here we aimed at identifying core areas for stimulus-context integration and delineated their functional connectivity (FC) using meta-analytic connectivity modeling (MACM) and analysis of resting-state networks. In a multi-study conjunction, consistently increased activity under higher demands on stimulus-context integration was predominantly found in the right temporo-parietal junction (TPJ), which represented the largest cluster of overlap and was thus used as the seed for the FC analyses. The conjunction between task-dependent (MACM) and task-free (resting state) FC of the right TPJ revealed a shared network comprising bilaterally inferior parietal and frontal cortices, anterior insula, premotor cortex, putamen and cerebellum, i.e., a 'ventral' action/attention network. Stronger task-dependent (vs. task-free) connectivity was observed with the pre-SMA, dorsal premotor cortex, intraparietal sulcus, basal ganglia and primary sensori motor cortex, while stronger resting-state (vs. task-dependent) connectivity was found with the dorsolateral prefrontal and medial parietal cortex. Our data provide strong evidence that the right TPJ may represent a key region for the integration of sensory stimuli and contextual frames in action control. Task-dependent associations with regions related to stimulus processing and motor responses indicate that the right TPJ may integrate 'collaterals' of sensory processing and apply (ensuing) contextual frames, most likely via modulation of preparatory loops. Given the pattern of resting-state connectivity, internal states and goal representations may provide the substrates for the contextual integration within the TPJ in the absence of a specific task.

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

[2]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

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

[4]  Marco Iacoboni,et al.  Fast Visuomotor Processing of Redundant Targets: The Role of the Right Temporo-Parietal Junction , 2008, PloS one.

[5]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[6]  A. Schleicher,et al.  Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus , 2006, The Journal of comparative neurology.

[7]  Angela R. Laird,et al.  Modelling neural correlates of working memory: A coordinate-based meta-analysis , 2012, NeuroImage.

[8]  Simon B Eickhoff,et al.  Dissociating bottom-up and top-down processes in a manual stimulus-response compatibility task. , 2010, Journal of neurophysiology.

[9]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[10]  Simon B. Eickhoff,et al.  Assignment of functional activations to probabilistic cytoarchitectonic areas revisited , 2007, NeuroImage.

[11]  K. Zilles,et al.  Neural correlates of developing and adapting behavioral biases in speeded choice reactions--an fMRI study on predictive motor coding. , 2011, Cerebral cortex.

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

[13]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[14]  Nicola Palomero-Gallagher,et al.  Subdivisions of human parietal area 5 revealed by quantitative receptor autoradiography: a parietal region between motor, somatosensory, and cingulate cortical areas , 2005, NeuroImage.

[15]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[16]  K. Zilles,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 2. Spatial Normalization to Standard Anatomical Space , 2000, NeuroImage.

[17]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[18]  Gereon R Fink,et al.  Differential involvement of the posterior temporal cortex in mentalizing but not perspective taking. , 2008, Social cognitive and affective neuroscience.

[19]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

[20]  Jacqueline Gottlieb,et al.  Spatial and non-spatial functions of the parietal cortex , 2010, Current Opinion in Neurobiology.

[21]  M. Corbetta,et al.  Interaction of Stimulus-Driven Reorienting and Expectation in Ventral and Dorsal Frontoparietal and Basal Ganglia-Cortical Networks , 2009, The Journal of Neuroscience.

[22]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[23]  Jon Driver,et al.  Integration of Goal- and Stimulus-Related Visual Signals Revealed by Damage to Human Parietal Cortex , 2010, The Journal of Neuroscience.

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

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

[26]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[27]  Karl J. Friston,et al.  Attention, Uncertainty, and Free-Energy , 2010, Front. Hum. Neurosci..

[28]  R. Passingham,et al.  Multiple Movement Representations in the Human Brain: An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[29]  Jessica A. Turner,et al.  Neuroinformatics Original Research Article , 2022 .

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

[31]  Katrin Amunts,et al.  Cytoarchitecture and probabilistic maps of the human posterior insular cortex. , 2010, Cerebral cortex.

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

[33]  D. Yves von Cramon,et al.  Bending the Rules: Strategic Behavioral Differences Are Reflected in the Brain , 2010, Journal of Cognitive Neuroscience.

[34]  T. Egner Congruency sequence effects and cognitive control , 2007, Cognitive, affective & behavioral neuroscience.

[35]  Jörn Diedrichsen,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[36]  Stefan Geyer,et al.  Prologue: Toward the Concept of a Cortical Control of Voluntary Movements , 2004 .

[37]  A. Schleicher,et al.  Receptor architecture of human cingulate cortex: Evaluation of the four‐region neurobiological model , 2009, Human brain mapping.

[38]  Dr. Stefan Geyer The Microstructural Border Between the Motor and the Cognitive Domain in the Human Cerebral Cortex , 2004, Advances in Anatomy Embryology and Cell Biology.

[39]  A. Schleicher,et al.  Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT+: a probabilistic, stereotaxic map of area hOc5. , 2006, Cerebral cortex.

[40]  J. Gottlieb From Thought to Action: The Parietal Cortex as a Bridge between Perception, Action, and Cognition , 2007, Neuron.

[41]  K. Zilles,et al.  Mind Reading: Neural Mechanisms of Theory of Mind and Self-Perspective , 2001, NeuroImage.

[42]  Karl Zilles,et al.  Cytology and receptor architecture of human anterior cingulate cortex , 2008, The Journal of comparative neurology.

[43]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[44]  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.

[45]  Karl J. Friston,et al.  The mirror-neuron system: a Bayesian perspective. , 2007, Neuroreport.

[46]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[47]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[48]  Glyn W. Humphreys,et al.  Author ' s personal copy Decomposing the neural mechanisms of visual search through model-based analysis of fMRI : Top-down excitation , active ignoring and the use of saliency by the right TPJ , 2012 .

[49]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[50]  Christopher Summerfield,et al.  Dissociable Neural Mechanisms for Encoding Predictable and Unpredictable Events , 2006, Journal of Cognitive Neuroscience.

[51]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[52]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

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

[54]  Synnöve Carlson,et al.  Multisensory Integration of Sounds and Vibrotactile Stimuli in Processing Streams for “What” and “Where” , 2009, The Journal of Neuroscience.

[55]  J. Smallwood,et al.  The restless mind. , 2006, Psychological bulletin.

[56]  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.

[57]  Habib Benali,et al.  Identification of large-scale networks in the brain using fMRI , 2006, NeuroImage.

[58]  Timothy Edward John Behrens,et al.  Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. , 2005, Cerebral cortex.

[59]  Simon B Eickhoff,et al.  Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses , 2012, Human brain mapping.

[60]  Philippe A. Chouinard,et al.  The Primary Motor and Premotor Areas of the Human Cerebral Cortex , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[61]  A. Schleicher,et al.  Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. , 2008, Cerebral cortex.

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

[63]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[64]  Marco Iacoboni,et al.  Visuo-motor integration and control in the human posterior parietal cortex: Evidence from TMS and fMRI , 2006, Neuropsychologia.

[65]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[66]  E. Koechlin,et al.  Broca's Area and the Hierarchical Organization of Human Behavior , 2006, Neuron.

[67]  E. M. Rouiller,et al.  Multisensory anatomical pathways , 2009, Hearing Research.

[68]  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.

[69]  S. Ferber,et al.  Spatial awareness is a function of the temporal not the posterior parietal lobe , 2001, Nature.

[70]  S. Funahashi,et al.  Thalamic mediodorsal nucleus and working memory , 2012, Neuroscience & Biobehavioral Reviews.

[71]  J. Müller,et al.  Of the brain. , 1837 .

[72]  G. Fink,et al.  Minds at rest? Social cognition as the default mode of cognizing and its putative relationship to the “default system” of the brain , 2008, Consciousness and Cognition.

[73]  K. Amunts,et al.  Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. , 2008, Cerebral cortex.

[74]  C. Spence,et al.  Crossmodal Space and Crossmodal Attention , 2004 .

[75]  A. Schleicher,et al.  The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. , 2006, Cerebral cortex.

[76]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[77]  C. Summerfield,et al.  An information theoretical approach to prefrontal executive function , 2007, Trends in Cognitive Sciences.

[78]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[79]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

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

[81]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[82]  Giuseppe Vallar,et al.  Deficits of position sense, unilateral neglect and optokinetic stimulation , 1993, Neuropsychologia.

[83]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[84]  K. Amunts,et al.  The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. , 2006, Cerebral cortex.

[85]  Simon B. Eickhoff,et al.  Effects of timing and movement uncertainty implicate the temporo-parietal junction in the prediction of forthcoming motor actions , 2009, NeuroImage.

[86]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[87]  Alois Schlögl,et al.  Analyzing event-related EEG data with multivariate autoregressive parameters. , 2006, Progress in brain research.

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

[89]  S. Aglioti,et al.  The body in the brain revisited , 2009, Experimental Brain Research.

[90]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

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

[92]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

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

[94]  Joshua I Gold,et al.  Correlates of Perceptual Learning in an Oculomotor Decision Variable , 2009, The Journal of Neuroscience.

[95]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[96]  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.