Parallel Distributed Networks Dissociate Episodic and Social Functions Within the Individual

Association cortex is organized into large-scale distributed networks. One such network, the default network (DN), is linked to diverse forms of internal mentation, opening debate about whether shared anatomy supports multiple forms of cognition. Alternatively, subtle distinctions in cortical organization could remain to be resolved. Using within-individual analysis procedures that preserve idiosyncratic details of cortical anatomy, we probed whether multiple tasks from two domains - Episodic Projection and Theory of Mind (ToM) - rely upon the same or distinct networks. In an initial experiment (n=6, subjects scanned 4 times each), we found evidence that Episodic Projection and ToM tasks activate distinct functional regions distributed throughout cortex, with adjacent regions in parietal, temporal, prefrontal and midline zones. These distinctions were predicted by the hypothesis that the DN comprises two parallel, interdigitated networks. One network, linked to parahippocampal cortex (PHC), is preferentially recruited during Episodic Projection, including both remembering the past and imagining the future. A second juxtaposed network, which includes the temporoparietal junction (TPJ), is differentially engaged during multiple forms of ToM tasks. The TPJ-linked network is interwoven with the PHC-linked network in multiple zones, including the posterior and anterior midline, making clear why it is difficult to fully resolve the two networks in group-averaged or lower-resolution data. We replicated all aspects of this network dissociation in a second, prospectively acquired dataset (n=6). These results refine our understanding of the functional-anatomical organization of association cortex as well as raise questions about how functional specialization might arise in parallel, juxtaposed association networks.

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

[2]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[3]  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.

[4]  Daniel S. Margulies,et al.  Macroscale cortical organization and a default-like apex transmodal network in the marmoset monkey , 2019, Nature Communications.

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

[6]  John W. Harwell,et al.  Similar patterns of cortical expansion during human development and evolution , 2010, Proceedings of the National Academy of Sciences.

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

[8]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

[9]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[10]  Donald T. Stuss,et al.  Common and Unique Neural Correlates of Autobiographical Memory and Theory of Mind , 2010, Journal of Cognitive Neuroscience.

[11]  Randy L. Buckner,et al.  Parallel distributed networks resolved at high resolution reveal close juxtaposition of distinct regions , 2018, bioRxiv.

[12]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[13]  Emile G. Bruneau,et al.  Distinct roles of the ‘Shared Pain’ and ‘Theory of Mind’ networks in processing others’ emotional suffering , 2012, Neuropsychologia.

[14]  Martial Van der Linden,et al.  Self-referential reflective activity and its relationship with rest: a PET study , 2005, NeuroImage.

[15]  Zachary C. Irving,et al.  Mind-wandering as spontaneous thought: a dynamic framework , 2016, Nature Reviews Neuroscience.

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

[17]  Rodrigo M. Braga,et al.  Parallel Interdigitated Distributed Networks within the Individual Estimated by Intrinsic Functional Connectivity , 2017, Neuron.

[18]  P. Goldman-Rakic Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[19]  Adrian W. Gilmore,et al.  Distinct subdivisions of human medial parietal cortex support recollection of people and places , 2019, eLife.

[20]  N. Kanwisher,et al.  New method for fMRI investigations of language: defining ROIs functionally in individual subjects. , 2010, Journal of neurophysiology.

[21]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[22]  Evan M. Gordon,et al.  Precision Functional Mapping of Individual Human Brains , 2017, Neuron.

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

[24]  Xi-Nian Zuo,et al.  Spatial Topography of Individual-Specific Cortical Networks Predicts Human Cognition, Personality, and Emotion. , 2019, Cerebral cortex.

[25]  Evan M. Gordon,et al.  Functional System and Areal Organization of a Highly Sampled Individual Human Brain , 2015, Neuron.

[26]  Margaret S Livingstone,et al.  Retinotopic Organization of Scene Areas in Macaque Inferior Temporal Cortex , 2017, The Journal of Neuroscience.

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

[28]  R. N. Spreng,et al.  The Future of Memory: Remembering, Imagining, and the Brain , 2012, Neuron.

[29]  R. Nathan Spreng,et al.  Patterns of Brain Activity Supporting Autobiographical Memory, Prospection, and Theory of Mind, and Their Relationship to the Default Mode Network , 2010, Journal of Cognitive Neuroscience.

[30]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[31]  Julia M. Huntenburg,et al.  Large-Scale Gradients in Human Cortical Organization , 2018, Trends in Cognitive Sciences.

[32]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

[33]  Evan M. Gordon,et al.  Long-term neural and physiological phenotyping of a single human , 2015, Nature Communications.

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

[35]  Olaf Blanke,et al.  Brain system for mental orientation in space, time, and person , 2015, Proceedings of the National Academy of Sciences.

[36]  Timothy O. Laumann,et al.  Informatics and Data Mining Tools and Strategies for the Human Connectome Project , 2011, Front. Neuroinform..

[37]  M. Livingstone,et al.  A hierarchical, retinotopic proto-organization of the primate visual system at birth , 2017, eLife.

[38]  Thomas L. Griffiths,et al.  Supplementary Information for Natural Speech Reveals the Semantic Maps That Tile Human Cerebral Cortex , 2022 .

[39]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[40]  R. Buckner,et al.  The brain’s default network: updated anatomy, physiology and evolving insights , 2019, Nature Reviews Neuroscience.

[41]  Rebecca Saxe,et al.  fMRI item analysis in a theory of mind task , 2011, NeuroImage.

[42]  Rebecca Saxe,et al.  Localizing Pain Matrix and Theory of Mind networks with both verbal and non-verbal stimuli , 2015, NeuroImage.

[43]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[44]  Jason P. Mitchell,et al.  Reading fiction and reading minds: the role of simulation in the default network. , 2016, Social cognitive and affective neuroscience.

[45]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[46]  Wen-Ming Luh,et al.  Multi-echo fMRI replication sample of autobiographical memory, prospection and theory of mind reasoning tasks , 2016, Scientific Data.

[47]  Matthew D. Lieberman,et al.  Social cognitive neuroscience: a review of core processes. , 2007, Annual review of psychology.

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

[49]  J. Polimeni,et al.  Blipped‐controlled aliasing in parallel imaging for simultaneous multislice echo planar imaging with reduced g‐factor penalty , 2012, Magnetic resonance in medicine.

[50]  Elizabeth Jefferies,et al.  Situating the default-mode network along a principal gradient of macroscale cortical organization , 2016, Proceedings of the National Academy of Sciences.

[51]  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.

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

[53]  Randy L. Buckner,et al.  The evolution of distributed association networks in the human brain , 2013, Trends in Cognitive Sciences.

[54]  Barbara G. Shinn-Cunningham,et al.  Short-Term Memory for Space and Time Flexibly Recruit Complementary Sensory-Biased Frontal Lobe Attention Networks , 2015, Neuron.

[55]  Brian Levine,et al.  Theory of Mind Is Independent of Episodic Memory , 2007, Science.

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

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

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

[59]  R. N. Spreng,et al.  The default network and self‐generated thought: component processes, dynamic control, and clinical relevance , 2014, Annals of the New York Academy of Sciences.

[60]  J. Perner,et al.  Neuroscience and Biobehavioral Reviews Fractionating Theory of Mind: a Meta-analysis of Functional Brain Imaging Studies , 2022 .

[61]  Nancy Kanwisher,et al.  Language-Selective and Domain-General Regions Lie Side by Side within Broca’s Area , 2012, Current Biology.

[62]  Rebecca Saxe,et al.  Contributions of episodic retrieval and mentalizing to autobiographical thought: Evidence from functional neuroimaging, resting-state connectivity, and fMRI meta-analyses , 2014, NeuroImage.