Subcortical Anatomy of the Default Mode Network: a functional and structural connectivity study

Most existing research into the default-mode network (DMN) has taken a corticocentric approach. Despite the resemblance of the DMN with the unitary model of the limbic system, the anatomy and contribution of subcortical structures to the network may be underappreciated due to methods limitation. Here, we propose a new and more comprehensive neuroanatomical model of the DMN including the basal forebrain and anterior and mediodorsal thalamic nuclei and cholinergic nuclei. This has been achieved by considering functional territories during interindividual brain alignment. Additionally, tractography of diffusion-weighted imaging was employed to explore the structural connectivity of the DMN and revealed that the thalamus and basal forebrain had high importance in term of values of node degree and centrality in the network. The contribution of these neurochemically diverse brain nuclei reconciles previous neuroimaging with neuropathological findings in diseased brain and offers the potential for identifying a conserved homologue of the DMN in other mammalian species.

[1]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[2]  M. Petrides,et al.  The Human Ventromedial Prefrontal Cortex: Sulcal Morphology and Its Influence on Functional Organization , 2019, The Journal of Neuroscience.

[3]  G. Varoquaux,et al.  Subspecialization within default mode nodes characterized in 10,000 UK Biobank participants , 2018, Proceedings of the National Academy of Sciences.

[4]  Leonardo Cerliani,et al.  Structural Variability Across the Primate Brain: A Cross-Species Comparison , 2018, Cerebral cortex.

[5]  Daniel S. Margulies,et al.  Macroscale Cortical Organization and a Default-Like Transmodal Apex Network in the Marmoset Monkey , 2018, bioRxiv.

[6]  B. Turetsky,et al.  Computing the Social Brain Connectome Across Systems and States , 2018, Cerebral cortex.

[7]  N. Tanriover,et al.  Mammillothalamic and Mammillotegmental Tracts as New Targets for Dementia and Epilepsy Treatment. , 2018, World neurosurgery.

[8]  G. Rainer,et al.  Basal forebrain contributes to default mode network regulation , 2018, Proceedings of the National Academy of Sciences.

[9]  Jian Wang,et al.  SOAPnuke: a MapReduce acceleration-supported software for integrated quality control and preprocessing of high-throughput sequencing data , 2017, GigaScience.

[10]  Richard Levy,et al.  Two critical brain networks for generation and combination of remote associations , 2018, Brain : a journal of neurology.

[11]  N. Volkow,et al.  Correlation between Traits of Emotion-Based Impulsivity and Intrinsic Default-Mode Network Activity , 2017, Neural plasticity.

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

[13]  R. Levy,et al.  Advanced lesion symptom mapping analyses and implementation as BCBtoolkit , 2017, bioRxiv.

[14]  P. Vernier,et al.  New perspective on the regionalization of the anterior forebrain in Osteichthyes , 2017, Development, growth & differentiation.

[15]  Xiujuan Geng,et al.  Salience and default mode network dysregulation in chronic cocaine users predict treatment outcome , 2017, Brain : a journal of neurology.

[16]  Xueling Zhu,et al.  Rumination and Default Mode Network Subsystems Connectivity in First-episode, Drug-Naive Young Patients with Major Depressive Disorder , 2017, Scientific Reports.

[17]  Elyssa B. Margolis,et al.  Ventral tegmental area: cellular heterogeneity, connectivity and behaviour , 2017, Nature Reviews Neuroscience.

[18]  T. Shallice,et al.  Identical, similar or different? Is a single brain model sufficient? , 2017, Cortex.

[19]  Sebastien Ourselin,et al.  The importance of correcting for signal drift in diffusion MRI , 2017, Magnetic resonance in medicine.

[20]  M Spies,et al.  Default mode network deactivation during emotion processing predicts early antidepressant response , 2017, Translational Psychiatry.

[21]  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.

[22]  P. Kalivas,et al.  The Nucleus Accumbens: Mechanisms of Addiction across Drug Classes Reflect the Importance of Glutamate Homeostasis , 2016, Pharmacological Reviews.

[23]  John P. Aggleton,et al.  Thalamic pathology and memory loss in early Alzheimer’s disease: moving the focus from the medial temporal lobe to Papez circuit , 2016, Brain : a journal of neurology.

[24]  Y. Okamoto,et al.  Association of thalamic hyperactivity with treatment-resistant depression and poor response in early treatment for major depression: a resting-state fMRI study using fractional amplitude of low-frequency fluctuations , 2016, Translational Psychiatry.

[25]  Yingjie Zhu,et al.  A thalamic input to the nucleus accumbens mediates opiate dependence , 2016, Nature.

[26]  Rebecca A Mease,et al.  Cortical Sensory Responses Are Enhanced by the Higher-Order Thalamus. , 2016, Cell reports.

[27]  P. Fox,et al.  Functional Segregation of the Human Dorsomedial Prefrontal Cortex. , 2016, Cerebral cortex.

[28]  Timothy O. Laumann,et al.  Generation and Evaluation of a Cortical Area Parcellation from Resting-State Correlations. , 2016, Cerebral cortex.

[29]  Carl-Fredrik Westin,et al.  The white matter query language: a novel approach for describing human white matter anatomy , 2015, Brain Structure and Function.

[30]  Harvey J Karten,et al.  Vertebrate brains and evolutionary connectomics: on the origins of the mammalian ‘neocortex’ , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  J. Pariente,et al.  Thalamic amnesia after infarct , 2015, Neurology.

[32]  Lesley A. McCollum,et al.  Uncovering the role of the nucleus accumbens in schizophrenia: A postmortem analysis of tyrosine hydroxylase and vesicular glutamate transporters , 2015, Schizophrenia Research.

[33]  Satrajit S. Ghosh,et al.  Predicting Activation Across Individuals with Resting-State Functional Connectivity Based Multi-Atlas Label Fusion , 2015, MICCAI.

[34]  S. Lehéricy,et al.  Hippocampal‐thalamic wiring in medial temporal lobe epilepsy: Enhanced connectivity per hippocampal voxel , 2015, Epilepsia.

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

[36]  Steve S. Chung,et al.  Long-term efficacy and safety of thalamic stimulation for drug-resistant partial epilepsy , 2015, Neurology.

[37]  J. Öhman,et al.  Defining the anterior nucleus of the thalamus (ANT) as a deep brain stimulation target in refractory epilepsy: Delineation using 3 T MRI and intraoperative microelectrode recording , 2015, NeuroImage: Clinical.

[38]  Wilfried Philips,et al.  MRI Segmentation of the Human Brain: Challenges, Methods, and Applications , 2015, Comput. Math. Methods Medicine.

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

[40]  S. Gentleman,et al.  Nucleus basalis of Meynert revisited: anatomy, history and differential involvement in Alzheimer’s and Parkinson’s disease , 2015, Acta Neuropathologica.

[41]  S. Floresco The nucleus accumbens: an interface between cognition, emotion, and action. , 2015, Annual review of psychology.

[42]  Z. Nadasdy,et al.  Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. , 2015, Cerebral cortex.

[43]  E. S. B. van Oort,et al.  An investigation into the functional and structural connectivity of the Default Mode Network , 2014, NeuroImage.

[44]  Kristina M. Visscher,et al.  Ventral Tegmental Area/Midbrain Functional Connectivity and Response to Antipsychotic Medication in Schizophrenia , 2014, Neuropsychopharmacology.

[45]  Massimo Silvetti,et al.  Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete virtual "in vivo" tractography dissection. , 2012, Cerebral cortex.

[46]  Steen Moeller,et al.  Evaluation of slice accelerations using multiband echo planar imaging at 3T , 2013, NeuroImage.

[47]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[48]  E. Benarroch,et al.  Anterior nucleus of the thalamus , 2013, Neurology.

[49]  M. Catani,et al.  Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true‐tract specific index to characterize white matter diffusion , 2013, Human brain mapping.

[50]  Michel Thiebaut de Schotten,et al.  A revised limbic system model for memory, emotion and behaviour , 2013, Neuroscience & Biobehavioral Reviews.

[51]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

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

[53]  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.

[54]  Glyn Humphreys,et al.  Mu rhythm desynchronization reveals motoric influences of hand action on object recognition , 2013, Front. Hum. Neurosci..

[55]  M. Fox,et al.  Individual Variability in Functional Connectivity Architecture of the Human Brain , 2013, Neuron.

[56]  E. Halgren,et al.  Septal nuclei enlargement in human temporal lobe epilepsy without mesial temporal sclerosis , 2013, Neurology.

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

[58]  MRI anatomical variants of mammillary bodies , 2013, Brain Structure and Function.

[59]  Fabrizio Esposito,et al.  Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease , 2012, Neurology.

[60]  R. Wise,et al.  Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens , 2012, Neuron.

[61]  N. Voets,et al.  Structural substrates for resting network disruption in temporal lobe epilepsy. , 2012, Brain : a journal of neurology.

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

[63]  G. Dai,et al.  Neuroanatomic Connectivity of the Human Ascending Arousal System Critical to Consciousness and Its Disorders , 2012, Journal of neuropathology and experimental neurology.

[64]  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.

[65]  Alan Connelly,et al.  MRtrix: Diffusion tractography in crossing fiber regions , 2012, Int. J. Imaging Syst. Technol..

[66]  M. Raichle,et al.  Rat brains also have a default mode network , 2012, Proceedings of the National Academy of Sciences.

[67]  Michel Thiebaut de Schotten,et al.  Short frontal lobe connections of the human brain , 2012, Cortex.

[68]  R. Buckner,et al.  The organization of the human striatum estimated by intrinsic functional connectivity. , 2012, Journal of neurophysiology.

[69]  Yong He,et al.  Diffusion tensor tractography reveals disrupted topological efficiency in white matter structural networks in multiple sclerosis. , 2011, Cerebral cortex.

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

[71]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[72]  Rita Z. Goldstein,et al.  Motivation Deficit in ADHD is Associated with Dysfunction of the Dopamine Reward Pathway , 2010, Molecular Psychiatry.

[73]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[74]  Stephen M. Smith,et al.  Multiplexed Echo Planar Imaging for Sub-Second Whole Brain FMRI and Fast Diffusion Imaging , 2010, PloS one.

[75]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[76]  K. Amunts,et al.  Reduction of basal forebrain cholinergic system parallels cognitive impairment in patients at high risk of developing Alzheimer's disease. , 2010, Cerebral cortex.

[77]  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.

[78]  Deanna L. Wallace,et al.  ΔFosB in brain reward circuits mediates resilience to stress and antidepressant responses , 2010, Nature Neuroscience.

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

[80]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[81]  M. Mallar Chakravarty,et al.  Morphological abnormalities of the thalamus in youths with attention deficit hyperactivity disorder. , 2010, The American journal of psychiatry.

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

[83]  Brian B. Avants,et al.  The optimal template effect in hippocampus studies of diseased populations , 2010, NeuroImage.

[84]  Giuseppe Scotti,et al.  A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution , 2010, NeuroImage.

[85]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[86]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[87]  Daniel S. Margulies,et al.  Functional connectivity of the human amygdala using resting state fMRI , 2009, NeuroImage.

[88]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[89]  S. Debener,et al.  Default-mode brain dysfunction in mental disorders: A systematic review , 2009, Neuroscience & Biobehavioral Reviews.

[90]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[91]  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.

[92]  Jeremy D. Schmahmann,et al.  Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies , 2009, NeuroImage.

[93]  Jan Sijbers,et al.  ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data , 2009 .

[94]  B. Biswal,et al.  Functional connectivity of human striatum: a resting state FMRI study. , 2008, Cerebral cortex.

[95]  Katrin Amunts,et al.  Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain , 2008, NeuroImage.

[96]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[97]  R. Salvador,et al.  Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network? , 2008, Psychological Medicine.

[98]  L. Nyberg,et al.  Altered deactivation in individuals with genetic risk for Alzheimer's disease , 2008, Neuropsychologia.

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

[100]  A. Butler Evolution of the thalamus: a morphological and functional review , 2008 .

[101]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[102]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[103]  Giuseppe Pagnoni,et al.  A comparison of resting-state brain activity in humans and chimpanzees , 2007, Proceedings of the National Academy of Sciences.

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

[105]  Ivan Osorio,et al.  High Frequency Thalamic Stimulation for Inoperable Mesial Temporal Epilepsy , 2007, Epilepsia.

[106]  R. Bluhm,et al.  Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. , 2007, Schizophrenia bulletin.

[107]  S. Laviolette Dopamine modulation of emotional processing in cortical and subcortical neural circuits: evidence for a final common pathway in schizophrenia? , 2007, Schizophrenia bulletin.

[108]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[109]  Richard C Saunders,et al.  Origin and topography of fibers contributing to the fornix in macaque monkeys , 2007, Hippocampus.

[110]  Tianzi Jiang,et al.  Regional coherence changes in the early stages of Alzheimer’s disease: A combined structural and resting-state functional MRI study , 2007, NeuroImage.

[111]  M. Hasselmo The role of acetylcholine in learning and memory , 2006, Current Opinion in Neurobiology.

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

[113]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[114]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[115]  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.

[116]  J. Gee,et al.  Geodesic estimation for large deformation anatomical shape averaging and interpolation , 2004, NeuroImage.

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

[118]  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.

[119]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[120]  M. Olmstead,et al.  Integrated contributions of basal forebrain and thalamus to neocortical activation elicited by pedunculopontine tegmental stimulation in urethane-anesthetized rats , 2003, Neuroscience.

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

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

[123]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[124]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[125]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

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

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

[128]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[129]  M. Corbetta,et al.  Top-down modulation of early sensory cortex. , 1997 .

[130]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[131]  R. Andersen,et al.  Posterior parietal cortex. , 1989, Reviews of oculomotor research.

[132]  D. Ingvar “Hyperfrontal” distribution of the cerebral grey matter flow in resting wakefulness; on the functional anatomy of the conscious state , 1979, Acta neurologica Scandinavica.

[133]  C. F. Brisseau de Mirbel,et al.  Traité d'anatomie et de physiologie végétales, suivi de la nomenclature méthodique ou raisonnée des parties extérieures des plantes, et un exposé succinct des systêmes de botanique les plus généralement adoptés. Ouvrage servant d'introduction a l'étude de la botanique ... , 1976 .

[134]  P. Yakovlev,et al.  Limbic nuclei of thalamus and connections of limbic cortex. III. Corticocortical connections of the anterior cingulate gyrus, the cingulum, and the subcallosal bundle in monkey. , 1961, Archives of neurology.

[135]  F CONTAMIN,et al.  [Temporal lobe epilepsy]. , 1954, La semaine des hopitaux : organe fonde par l'Association d'enseignement medical des hopitaux de Paris.

[136]  P. Maclean Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). , 1952, Electroencephalography and clinical neurophysiology.

[137]  P. Maclean Psychosomatic Disease and the "Visceral Brain": Recent Developments Bearing on the Papez Theory of Emotion , 1949, Psychosomatic medicine.

[138]  P. Yakovlev MOTILITY, BEHAVIOR AND THE BRAIN*: STEREODYNAMIC ORGANIZATION AND NEURAL CO‐ORDINATES OF BEHAVIOR , 1948, The Journal of nervous and mental disease.

[139]  J. W. Papez A PROPOSED MECHANISM OF EMOTION , 1937 .