The default network and the combination of cognitive processes that mediate self-generated thought

Self-generated cognitions, such as recalling personal memories or empathizing with others, are ubiquitous and essential for our lives. Such internal mental processing is ascribed to the default mode network—a large network of the human brain—although the underlying neural and cognitive mechanisms remain poorly understood. Here, we tested the hypothesis that our mental experience is mediated by a combination of activities of multiple cognitive processes. Our study included four functional magnetic resonance imaging experiments with the same participants and a wide range of cognitive tasks, as well as an analytical approach that afforded the identification of cognitive processes during self-generated cognition. We showed that several cognitive processes functioned simultaneously during self-generated mental activity. The processes had specific and localized neural representations, suggesting that they support different aspects of internal processing. Overall, we demonstrate that internally directed experience may be achieved by pooling over multiple cognitive processes.Over four functional MRI experiments, Axelrod et al. show that several cognitive processes function simultaneously during self-generated mental activity.

[1]  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.

[2]  C. Honey,et al.  Hierarchical process memory: memory as an integral component of information processing , 2015, Trends in Cognitive Sciences.

[3]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

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

[5]  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.

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

[7]  Gina F. Humphreys,et al.  Establishing task- and modality-dependent dissociations between the semantic and default mode networks , 2015, Proceedings of the National Academy of Sciences.

[8]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[9]  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.

[10]  A. Friederici The brain basis of language processing: from structure to function. , 2011, Physiological reviews.

[11]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[12]  Radoslaw Martin Cichy,et al.  Imagery and perception share cortical representations of content and location. , 2012, Cerebral Cortex.

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

[14]  Elizabeth Jefferies,et al.  Tracking thoughts: Exploring the neural architecture of mental time travel during mind-wandering , 2017, NeuroImage.

[15]  Lars A. Ross,et al.  What's unique about unique entities? An fMRI investigation of the semantics of famous faces and landmarks. , 2012, Cerebral cortex.

[16]  G. Winocur,et al.  Brain regions involved in the retrieval of spatial and episodic details associated with a familiar environment: An fMRI study , 2012, Neuropsychologia.

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

[18]  Alana T. Wong,et al.  Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration , 2007, Neuropsychologia.

[19]  Arnaud D'Argembeau,et al.  Neural correlates of personal goal processing during episodic future thinking and mind‐wandering: An ALE meta‐analysis , 2015, Human brain mapping.

[20]  Hao-Ting Wang,et al.  Varieties of semantic cognition revealed through simultaneous decomposition of intrinsic brain connectivity and behaviour , 2017, NeuroImage.

[21]  Russell A. Poldrack,et al.  Scanning the Horizon: Towards transparent and reproducible neuroimaging research , 2016 .

[22]  D. Hassabis,et al.  Patients with hippocampal amnesia cannot imagine new experiences , 2007, Proceedings of the National Academy of Sciences.

[23]  Jeffrey M. Zacks,et al.  Searchlight analysis: Promise, pitfalls, and potential , 2013, NeuroImage.

[24]  Demis Hassabis,et al.  Cortical midline involvement in autobiographical memory , 2009, NeuroImage.

[25]  S. Bookheimer Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[26]  Michael C. Corballis,et al.  The Wandering Mind , 2016 .

[27]  D. Gilbert,et al.  A Wandering Mind Is an Unhappy Mind , 2010, Science.

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

[29]  Rebecca Saxe,et al.  Associations and dissociations between default and self-reference networks in the human brain , 2011, NeuroImage.

[30]  A. Koeppen,et al.  Principles of Frontal Lobe Function, second ed., Donald T. Stuss, Robert T. Knight (Eds.). Oxford University Press, New York NY (2013), 800, pages, ISBN: 978-0-19-983775-5 , 2014 .

[31]  M Moscovitch,et al.  Similarities and differences in the default mode network across rest, retrieval, and future imagining , 2017, Human brain mapping.

[32]  Rodrigo M. Braga,et al.  Echoes of the Brain within the Posterior Cingulate Cortex , 2012, The Journal of Neuroscience.

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

[34]  M. Corbetta,et al.  Episodic Memory Retrieval, Parietal Cortex, and the Default Mode Network: Functional and Topographic Analyses , 2011, The Journal of Neuroscience.

[35]  I. Fried,et al.  A Widely Distributed Spectral Signature of Task-Negative Electrocorticography Responses Revealed during a Visuomotor Task in the Human Cortex , 2012, The Journal of Neuroscience.

[36]  Xu Lei,et al.  Activation and Connectivity within the Default Mode Network Contribute Independently to Future-Oriented Thought , 2016, Scientific Reports.

[37]  S. Thompson-Schill,et al.  Reworking the language network , 2014, Trends in Cognitive Sciences.

[38]  Vadim Axelrod On the domain‐specificity of the visual and non‐visual face‐selective regions , 2016, The European journal of neuroscience.

[39]  Christian F. Doeller,et al.  Establishing the Boundaries: The Hippocampal Contribution to Imagining Scenes , 2010, The Journal of Neuroscience.

[40]  Yuan Chang Leong,et al.  Shared memories reveal shared structure in neural activity across individuals , 2016, Nature Neuroscience.

[41]  Geraint Rees,et al.  Neural Correlates of Subliminal Language Processing , 2014, Cerebral cortex.

[42]  Li Fei-Fei,et al.  Two Distinct Scene-Processing Networks Connecting Vision and Memory , 2016, eNeuro.

[43]  R. Buckner,et al.  Opinion TRENDS in Cognitive Sciences Vol.11 No.2 Self-projection and the brain , 2022 .

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

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

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

[47]  Robert M. Kessler,et al.  Midbrain Dopamine Receptor Availability Is Inversely Associated with Novelty-Seeking Traits in Humans , 2008, The Journal of Neuroscience.

[48]  Thomas Serre,et al.  Reading the mind's eye: Decoding category information during mental imagery , 2010, NeuroImage.

[49]  D. Schacter,et al.  Constructive episodic simulation of the future and the past: Distinct subsystems of a core brain network mediate imagining and remembering , 2009, Neuropsychologia.

[50]  Naama Mayseless,et al.  Generating original ideas: The neural underpinning of originality , 2015, NeuroImage.

[51]  Jessica R. Andrews-Hanna,et al.  The Default Network and Social Cognition , 2015 .

[52]  M. Seghier The Angular Gyrus , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[53]  M. Verfaellie,et al.  Medial Temporal Lobe Contributions to Episodic Future Thinking: Scene Construction or Future Projection? , 2018, Cerebral cortex.

[54]  R. Malach,et al.  When the Brain Loses Its Self: Prefrontal Inactivation during Sensorimotor Processing , 2006, Neuron.

[55]  Bernard Mazoyer,et al.  Patterns of hemodynamic low-frequency oscillations in the brain are modulated by the nature of free thought during rest , 2012, NeuroImage.

[56]  Daniel S. Margulies,et al.  Delineating self-referential processing from episodic memory retrieval: Common and dissociable networks , 2010, NeuroImage.

[57]  Kaia L. Vilberg,et al.  Brain Networks Underlying Episodic Memory Retrieval This Review Comes from a Themed Issue on Macrocircuits Memory Signals within the Mtl , 2022 .

[58]  Marco Catani,et al.  Brain Mapping: An encyclopedic reference , 2015 .

[59]  D. Schacter,et al.  Specifying the core network supporting episodic simulation and episodic memory by activation likelihood estimation , 2015, Neuropsychologia.

[60]  Nikolaus Kriegeskorte,et al.  Pattern‐information fMRI: New questions which it opens up and challenges which face it , 2010, Int. J. Imaging Syst. Technol..

[61]  R. Nathan Spreng,et al.  The wandering brain: Meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes , 2015, NeuroImage.

[62]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[63]  J. Smallwood,et al.  That’s me in the spotlight: neural basis of individual differences in self-consciousness , 2017, Social cognitive and affective neuroscience.

[64]  Neal J. Cohen,et al.  Differential contributions of hippocampus and medial prefrontal cortex to self-projection and self-referential processing , 2015, Neuropsychologia.

[65]  Elizabeth Jefferies,et al.  How do we decide what to do? Resting-state connectivity patterns and components of self-generated thought linked to the development of more concrete personal goals , 2016, Experimental Brain Research.

[66]  Johan Wessberg,et al.  A Monte Carlo method for locally multivariate brain mapping , 2011, NeuroImage.

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

[68]  K. Christoff,et al.  Experience sampling during fMRI reveals default network and executive system contributions to mind wandering , 2009, Proceedings of the National Academy of Sciences.

[69]  L. Squire,et al.  Memory, scene construction, and the human hippocampus , 2015, Proceedings of the National Academy of Sciences.

[70]  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.

[71]  J. Smallwood,et al.  Automatic and Controlled Semantic Retrieval: TMS Reveals Distinct Contributions of Posterior Middle Temporal Gyrus and Angular Gyrus , 2015, The Journal of Neuroscience.

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

[73]  William M. Kelley,et al.  What Can the Organization of the Brain’s Default Mode Network Tell us About Self-Knowledge? , 2013, Front. Hum. Neurosci..

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

[75]  Elizabeth Jefferies,et al.  Down but not out in posterior cingulate cortex: Deactivation yet functional coupling with prefrontal cortex during demanding semantic cognition , 2016, NeuroImage.

[76]  Maurizio Corbetta,et al.  The contribution of the human posterior parietal cortex to episodic memory , 2017, Nature Reviews Neuroscience.

[77]  Melanie R. Silverman,et al.  Self-regulation via neural simulation , 2016, Proceedings of the National Academy of Sciences.

[78]  O. Piguet,et al.  The Pivotal Role of Semantic Memory in Remembering the Past and Imagining the Future , 2013, Front. Behav. Neurosci..

[79]  Rafael Malach,et al.  Stimulus-free thoughts induce differential activation in the human default network , 2011, NeuroImage.

[80]  Steve Majerus,et al.  The Neural Basis of Personal Goal Processing When Envisioning Future Events , 2010, Journal of Cognitive Neuroscience.

[81]  Anjali Krishnan,et al.  Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations , 2014, NeuroImage.

[82]  E. Tulving,et al.  Consciousness of subjective time in the brain , 2010, Proceedings of the National Academy of Sciences.

[83]  Boris C. Bernhardt,et al.  Classifying the wandering mind: Revealing the affective content of thoughts during task-free rest periods , 2014, NeuroImage.

[84]  Alison J. Wiggett,et al.  Surface-Based Information Mapping Reveals Crossmodal Vision–Action Representations in Human Parietal and Occipitotemporal Cortex , 2010, Journal of neurophysiology.

[85]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[86]  Hongkeun Kim,et al.  Default network activation during episodic and semantic memory retrieval: A selective meta-analytic comparison , 2016, Neuropsychologia.

[87]  B. Harrison,et al.  Consistency and functional specialization in the default mode brain network , 2008, Proceedings of the National Academy of Sciences.

[88]  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.

[89]  B. Foster,et al.  Intrinsic and Task-Dependent Coupling of Neuronal Population Activity in Human Parietal Cortex , 2015, Neuron.

[90]  Hao-Ting Wang,et al.  Representing Representation: Integration between the Temporal Lobe and the Posterior Cingulate Influences the Content and Form of Spontaneous Thought , 2016, PloS one.

[91]  G. Yovel,et al.  Successful Decoding of Famous Faces in the Fusiform Face Area , 2015, PloS one.

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

[93]  Daniel P. Kennedy,et al.  Differential electrophysiological response during rest, self-referential, and non–self-referential tasks in human posteromedial cortex , 2011, Proceedings of the National Academy of Sciences.

[94]  N. Kriegeskorte,et al.  Author ' s personal copy Representational geometry : integrating cognition , computation , and the brain , 2013 .

[95]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[96]  Todd F. Heatherton,et al.  Representational Similarity of Social and Valence Information in the Medial pFC , 2015, Journal of Cognitive Neuroscience.

[97]  Li Fei-Fei,et al.  Two distinct scene processing networks connecting vision and memory , 2016, bioRxiv.

[98]  Daniel S. Margulies,et al.  A Correspondence between Individual Differences in the Brain's Intrinsic Functional Architecture and the Content and Form of Self-Generated Thoughts , 2014, PloS one.

[99]  J. Smallwood,et al.  The science of mind wandering: empirically navigating the stream of consciousness. , 2015, Annual review of psychology.

[100]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[101]  M. Seghier,et al.  Functional Subdivisions in the Left Angular Gyrus Where the Semantic System Meets and Diverges from the Default Network , 2010, The Journal of Neuroscience.

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

[103]  Russell A. Epstein Parahippocampal and retrosplenial contributions to human spatial navigation , 2008, Trends in Cognitive Sciences.

[104]  Geraint Rees,et al.  Increasing propensity to mind-wander with transcranial direct current stimulation , 2015, Proceedings of the National Academy of Sciences.

[105]  N. Kanwisher,et al.  Mental Imagery of Faces and Places Activates Corresponding Stimulus-Specific Brain Regions , 2000, Journal of Cognitive Neuroscience.

[106]  Vadim Axelrod,et al.  Minimizing bugs in cognitive neuroscience programming , 2014, Front. Psychol..

[107]  M. Bar,et al.  The units of thought , 2007, Hippocampus.

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

[109]  Li Su,et al.  A Toolbox for Representational Similarity Analysis , 2014, PLoS Comput. Biol..

[110]  Xi-Nian Zuo,et al.  REST: A Toolkit for Resting-State Functional Magnetic Resonance Imaging Data Processing , 2011, PloS one.

[111]  Jennifer S. Rabin,et al.  Familiarity modulates the functional relationship between theory of mind and autobiographical memory , 2012, NeuroImage.

[112]  Cheryl L. Grady,et al.  Common and Unique Neural Activations in Autobiographical, Episodic, and Semantic Retrieval , 2007, Journal of Cognitive Neuroscience.

[113]  D. Hassabis,et al.  Using Imagination to Understand the Neural Basis of Episodic Memory , 2007, The Journal of Neuroscience.

[114]  Angela R. Laird,et al.  Subspecialization in the human posterior medial cortex , 2015, NeuroImage.

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

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

[117]  John A. E. Anderson,et al.  A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. , 2010, Cerebral cortex.

[118]  Steve Majerus,et al.  Neural Correlates of Ongoing Conscious Experience: Both Task-Unrelatedness and Stimulus-Independence Are Related to Default Network Activity , 2011, PloS one.

[119]  Robin W. Wilkins,et al.  Creativity and the default network: A functional connectivity analysis of the creative brain at rest , 2014, Neuropsychologia.

[120]  Rafael Malach,et al.  Deconstructing the default: Cortical subdivision of the default mode/intrinsic system during self‐related processing , 2014, Human brain mapping.

[121]  Rodrigo M. Braga,et al.  Echoes of the Brain within Default Mode, Association, and Heteromodal Cortices , 2013, The Journal of Neuroscience.

[122]  G. Yovel,et al.  Hierarchical Processing of Face Viewpoint in Human Visual Cortex , 2012, The Journal of Neuroscience.

[123]  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.

[124]  Nikolaus Kriegeskorte,et al.  Pattern-information fMRI: New questions which it opens up and challenges which face it , 2010 .

[125]  M. Bar,et al.  The role of the parahippocampal cortex in cognition , 2013, Trends in Cognitive Sciences.

[126]  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.

[127]  Marie Schaer,et al.  Degrees of separation: A quantitative neuroimaging meta-analysis investigating self-specificity and shared neural activation between self- and other-reflection , 2012, Neuroscience & Biobehavioral Reviews.

[128]  J. Smallwood Distinguishing how from why the mind wanders: a process-occurrence framework for self-generated mental activity. , 2013, Psychological bulletin.

[129]  D. Yves von Cramon,et al.  Thinking about the future versus the past in personal and non-personal contexts , 2008, Brain Research.

[130]  Janice Chen,et al.  Dynamic reconfiguration of the default mode network during narrative comprehension , 2016, Nature Communications.

[131]  Miranka Wirth,et al.  Semantic memory involvement in the default mode network: A functional neuroimaging study using independent component analysis , 2011, NeuroImage.

[132]  M. Raichle The brain's default mode network. , 2015, Annual review of neuroscience.

[133]  T. Hendler,et al.  Portraying the unique contribution of the default mode network to internally driven mnemonic processes , 2013, Proceedings of the National Academy of Sciences.

[134]  Amir Amedi,et al.  Massive cortical reorganization in sighted Braille readers , 2016, eLife.

[135]  Amanda V. Utevsky,et al.  Precuneus Is a Functional Core of the Default-Mode Network , 2014, The Journal of Neuroscience.

[136]  C. Neil Macrae,et al.  The Link between Social Cognition and Self-referential Thought in the Medial Prefrontal Cortex , 2005, Journal of Cognitive Neuroscience.

[137]  Hao-Ting Wang,et al.  The role of the default mode network in component processes underlying the wandering mind , 2017, Social cognitive and affective neuroscience.

[138]  Hongkeun Kim,et al.  A dual-subsystem model of the brain's default network: Self-referential processing, memory retrieval processes, and autobiographical memory retrieval , 2012, NeuroImage.

[139]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[140]  R. Nathan Spreng,et al.  Neural congruence between intertemporal and interpersonal self-control: Evidence from delay and social discounting , 2017, NeuroImage.

[141]  Tianzi Jiang,et al.  Changes in hippocampal connectivity in the early stages of Alzheimer's disease: Evidence from resting state fMRI , 2006, NeuroImage.

[142]  D. Sharp,et al.  Fractionating the Default Mode Network: Distinct Contributions of the Ventral and Dorsal Posterior Cingulate Cortex to Cognitive Control , 2011, The Journal of Neuroscience.

[143]  Rafael Malach,et al.  Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. , 2007, Cerebral cortex.

[144]  Paul Hoffman,et al.  The Semantic Network at Work and Rest: Differential Connectivity of Anterior Temporal Lobe Subregions , 2016, The Journal of Neuroscience.

[145]  K. Szpunar,et al.  Neural substrates of envisioning the future , 2007, Proceedings of the National Academy of Sciences.

[146]  E. Tulving Chronesthesia: Conscious awareness of subjective time. , 2002 .

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

[148]  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.