Definition and characterization of an extended social-affective default network

Recent evidence suggests considerable overlap between the default mode network (DMN) and regions involved in social, affective and introspective processes. We considered these overlapping regions as the social-affective part of the DMN. In this study, we established a robust mapping of the underlying brain network formed by these regions and those strongly connected to them (the extended social-affective default network). We first seeded meta-analytic connectivity modeling and resting-state analyses in the meta-analytically defined DMN regions that showed statistical overlap with regions associated with social and affective processing. Consensus connectivity of each seed was subsequently delineated by a conjunction across both connectivity analyses. We then functionally characterized the ensuing regions and performed several cluster analyses. Among the identified regions, the amygdala/hippocampus formed a cluster associated with emotional processes and memory functions. The ventral striatum, anterior cingulum, subgenual cingulum and ventromedial prefrontal cortex formed a heterogeneous subgroup associated with motivation, reward and cognitive modulation of affect. Posterior cingulum/precuneus and dorsomedial prefrontal cortex were associated with mentalizing, self-reference and autobiographic information. The cluster formed by the temporo-parietal junction and anterior middle temporal sulcus/gyrus was associated with language and social cognition. Taken together, the current work highlights a robustly interconnected network that may be central to introspective, socio-affective, that is, self- and other-related mental processes.

[1]  Thomas Dierks,et al.  Reduced Cerebral Blood Flow Within the Default-Mode Network and Within Total Gray Matter in Major Depression , 2012, Brain Connect..

[2]  G. Dimaggio,et al.  Know yourself and you shall know the other… to a certain extent: Multiple paths of influence of self-reflection on mindreading , 2008, Consciousness and Cognition.

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

[4]  J. A. Hartigan,et al.  A k-means clustering algorithm , 1979 .

[5]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[6]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[7]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[8]  John Suckling,et al.  Shared Neural Circuits for Mentalizing about the Self and Others , 2010, Journal of Cognitive Neuroscience.

[9]  Clement Hamani,et al.  The Subcallosal Cingulate Gyrus in the Context of Major Depression , 2011, Biological Psychiatry.

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

[11]  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.

[12]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

[13]  Angela R. Laird,et al.  Across-study and within-subject functional connectivity of a right temporo-parietal junction subregion involved in stimulus–context integration , 2012, NeuroImage.

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

[15]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

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

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

[18]  Cathy J. Price,et al.  Functional Heterogeneity within the Default Network during Semantic Processing and Speech Production , 2012, Front. Psychology.

[19]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[20]  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.

[21]  R. Buckner,et al.  Evidence for the Default Network's Role in Spontaneous Cognition , 2010 .

[22]  Steven Laureys,et al.  Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. , 2005, Progress in brain research.

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

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

[25]  O. Hikosaka,et al.  The Primate Ventral Pallidum Encodes Expected Reward Value and Regulates Motor Action , 2012, Neuron.

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

[27]  Nadim Joni Shah,et al.  Minds Made for Sharing: Initiating Joint Attention Recruits Reward-related Neurocircuitry , 2010, Journal of Cognitive Neuroscience.

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

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

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

[31]  P. Fox,et al.  Segregation of the human medial prefrontal cortex in social cognition , 2013, Front. Hum. Neurosci..

[32]  V. Menon Large-scale brain networks and psychopathology: a unifying triple network model , 2011, Trends in Cognitive Sciences.

[33]  Sterling C. Johnson,et al.  Neural correlates of self-reflection. , 2002, Brain : a journal of neurology.

[34]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

[35]  O. Blanke,et al.  The Out-of-Body Experience: Disturbed Self-Processing at the Temporo-Parietal Junction , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[36]  M. Bar The proactive brain: using analogies and associations to generate predictions , 2007, Trends in Cognitive Sciences.

[37]  L. Pessoa How do emotion and motivation direct executive control? , 2009, Trends in Cognitive Sciences.

[38]  A. Bechara,et al.  Cerebral Cortex doi:10.1093/cercor/bhn147 Functional Dissociations of Risk and Reward Processing in the Medial Prefrontal Cortex , 2008 .

[39]  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.

[40]  Karine Sergerie,et al.  The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies , 2008, Neuroscience & Biobehavioral Reviews.

[41]  Henrik Walter,et al.  Functional relations of empathy and mentalizing: An fMRI study on the neural basis of cognitive empathy , 2011, NeuroImage.

[42]  D. Schacter,et al.  Remembering the past to imagine the future: the prospective brain , 2007, Nature Reviews Neuroscience.

[43]  S. Eickhoff,et al.  Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. , 2013, Psychological bulletin.

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

[45]  Danilo Bzdok,et al.  The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data , 2011, BMC Research Notes.

[46]  R. Kahn,et al.  Lateralization of amygdala activation: a systematic review of functional neuroimaging studies , 2004, Brain Research Reviews.

[47]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

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

[49]  Angela R. Laird,et al.  Characterization of the temporo-parietal junction by combining data-driven parcellation, complementary connectivity analyses, and functional decoding , 2013, NeuroImage.

[50]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[51]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[52]  Simon B. Eickhoff,et al.  An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data , 2013, NeuroImage.

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

[54]  Peter Fransson,et al.  The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis , 2008, NeuroImage.

[55]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[56]  Angela R. Laird,et al.  Investigating function and connectivity of morphometric findings — Exemplified on cerebellar atrophy in spinocerebellar ataxia 17 (SCA17) , 2012, NeuroImage.

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

[58]  Istvan Molnar-Szakacs,et al.  Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline , 2004, NeuroImage.

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

[60]  Ivan Toni,et al.  On the relationship between the “default mode network” and the “social brain” , 2012, Front. Hum. Neurosci..

[61]  Angela R. Laird,et al.  Task- and resting-state functional connectivity of brain regions related to affection and susceptible to concurrent cognitive demand , 2013, NeuroImage.

[62]  M. Corbetta,et al.  Human cortical mechanisms of visual attention during orienting and search. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  Simon B. Eickhoff,et al.  Resting State Functional Connectivity in Patients with Chronic Hallucinations , 2012, PloS one.

[64]  M. Furey,et al.  Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression , 2008, Brain Structure and Function.

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

[66]  E. Phelps Human emotion and memory: interactions of the amygdala and hippocampal complex , 2004, Current Opinion in Neurobiology.

[67]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[68]  W. Schultz Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

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

[70]  Gal Meiri,et al.  Cortical activation during delay discounting in abstinent methamphetamine dependent individuals , 2008, Psychopharmacology.

[71]  Axel Cleeremans,et al.  Higher order thoughts in action: consciousness as an unconscious re-description process , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[73]  A. Todorov,et al.  The neural dynamics of updating person impressions. , 2013, Social cognitive and affective neuroscience.

[74]  E. Forgy,et al.  Cluster analysis of multivariate data : efficiency versus interpretability of classifications , 1965 .

[75]  J. Allman,et al.  The Anterior Cingulate Cortex , 2001, Annals of the New York Academy of Sciences.

[76]  Jan Derrfuss,et al.  Lost in localization: The need for a universal coordinate database , 2009, NeuroImage.

[77]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[78]  Simon B. Eickhoff,et al.  Meta-analytical definition and functional connectivity of the human vestibular cortex , 2012, NeuroImage.

[79]  E. Rolls,et al.  How the brain represents the reward value of fat in the mouth. , 2010, Cerebral cortex.

[80]  Lindsey J. Powell,et al.  It's the Thought That Counts , 2006, Psychological science.

[81]  M. Costandi Default Mode Network , 2015 .

[82]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[83]  U. Hasson,et al.  Speaker–listener neural coupling underlies successful communication , 2010, Proceedings of the National Academy of Sciences.

[84]  Reginald B. Adams,et al.  Cross-cultural Reading the Mind in the Eyes: An fMRI Investigation , 2010, Journal of Cognitive Neuroscience.

[85]  K. Vogeley,et al.  Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy , 2012, Brain Structure and Function.

[86]  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.

[87]  P. Fox,et al.  Introspective Minds: Using ALE Meta-Analyses to Study Commonalities in the Neural Correlates of Emotional Processing, Social & Unconstrained Cognition , 2012, PloS one.

[88]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[89]  A. Laird,et al.  The Neural Basis of Drug Stimulus Processing and Craving: An Activation Likelihood Estimation Meta-Analysis , 2011, Biological Psychiatry.

[90]  B. Gold,et al.  Functional Dissociation in Frontal and Striatal Areas for Processing of Positive and Negative Reward Information , 2007, The Journal of Neuroscience.

[91]  Georg Northoff,et al.  How is our self related to midline regions and the default-mode network? , 2011, NeuroImage.

[92]  Chad E. Forbes,et al.  The role of the human prefrontal cortex in social cognition and moral judgment. , 2010, Annual review of neuroscience.

[93]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

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

[95]  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.

[96]  Kevin N. Ochsner,et al.  A Meta-analysis of Functional Neuroimaging Studies of Self- and Other Judgments Reveals a Spatial Gradient for Mentalizing in Medial Prefrontal Cortex , 2012, Journal of Cognitive Neuroscience.

[97]  R. Adolphs,et al.  Impaired declarative memory for emotional material following bilateral amygdala damage in humans. , 1997, Learning & memory.

[98]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

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