Integrative and Network-Specific Connectivity of the Basal Ganglia and Thalamus Defined in Individuals

The basal ganglia, thalamus, and cerebral cortex form an interconnected network implicated in many neurological and psychiatric illnesses. A better understanding of cortico-subcortical circuits in individuals will aid in development of personalized treatments. Using precision functional mapping-individual-specific analysis of highly sampled human participants-we investigated individual-specific functional connectivity between subcortical structures and cortical functional networks. This approach revealed distinct subcortical zones of network specificity and multi-network integration. Integration zones were systematic, with convergence of cingulo-opercular control and somatomotor networks in the ventral intermediate thalamus (motor integration zones), dorsal attention and visual networks in the pulvinar, and default mode and multiple control networks in the caudate nucleus. The motor integration zones were present in every individual and correspond to consistently successful sites of deep brain stimulation (DBS; essential tremor). Individually variable subcortical zones correspond to DBS sites with less consistent treatment effects, highlighting the importance of PFM for neurosurgery, neurology, and psychiatry.

[1]  Ulman Lindenberger,et al.  Local temporal variability reflects functional integration in the human brain , 2018, NeuroImage.

[2]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  M. D’Esposito,et al.  Functional Characterization of the Cingulo-Opercular Network in the Maintenance of Tonic Alertness. , 2015, Cerebral cortex.

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

[5]  Elisabeth J. Ploran,et al.  Distinct Stages of Moment‐to‐Moment Processing in the Cinguloopercular and Frontoparietal Networks , 2017, Cerebral cortex.

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

[7]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[8]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[9]  Aaron S. Heller,et al.  Cortical-Subcortical Interactions in Depression: From Animal Models to Human Psychopathology , 2016, Front. Syst. Neurosci..

[10]  M. Delong,et al.  Deep-Brain Stimulation for Basal Ganglia Disorders. , 2011, Basal ganglia.

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

[12]  Jonathan D. Power,et al.  Evidence for Hubs in Human Functional Brain Networks , 2013, Neuron.

[13]  Daniel J Mitchell,et al.  Task Encoding across the Multiple Demand Cortex Is Consistent with a Frontoparietal and Cingulo-Opercular Dual Networks Distinction , 2016, The Journal of Neuroscience.

[14]  M. Chun,et al.  Functional connectome fingerprinting: Identifying individuals based on patterns of brain connectivity , 2015, Nature Neuroscience.

[15]  N. Swindale,et al.  Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans , 2004, Annals of neurology.

[16]  Jonathan D. Power,et al.  Identifying Basal Ganglia Divisions in Individuals Using Resting-State Functional Connectivity MRI , 2010, Front. Syst. Neurosci..

[17]  Andrew T. Drysdale,et al.  Resting-state connectivity biomarkers define neurophysiological subtypes of depression , 2016, Nature Medicine.

[18]  Pierre-François D'Haese,et al.  The Optimal Pallidal Target in Deep Brain Stimulation for Dystonia: A Study Using a Functional Atlas Based on Nonlinear Image Registration , 2014, Stereotactic and Functional Neurosurgery.

[19]  Siobhan Ewert,et al.  Lead-DBS v2: Towards a comprehensive pipeline for deep brain stimulation imaging , 2018, NeuroImage.

[20]  S. Shipp The brain circuitry of attention , 2004, Trends in Cognitive Sciences.

[21]  T. Verstynen,et al.  Converging Structural and Functional Connectivity of Orbitofrontal, Dorsolateral Prefrontal, and Posterior Parietal Cortex in the Human Striatum , 2014, The Journal of Neuroscience.

[22]  Christos Davatzikos,et al.  Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity , 2017, NeuroImage.

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

[24]  K. Hwang,et al.  The Contribution of Network Organization and Integration to the Development of Cognitive Control , 2015, PLoS biology.

[25]  Steven E Petersen,et al.  Tasks Driven by Perceptual Information Do Not Recruit Sustained BOLD Activity in Cingulo-Opercular Regions. , 2016, Cerebral cortex.

[26]  Joseph W. Dubis,et al.  Spatial and Temporal Characteristics of Error-Related Activity in the Human Brain , 2015, The Journal of Neuroscience.

[27]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[28]  L. Glass Moiré Effect from Random Dots , 1969, Nature.

[29]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[30]  I. Skogseid,et al.  Dystonia – new advances in classification, genetics, pathophysiology and treatment , 2014, Acta neurologica Scandinavica. Supplementum.

[31]  Andreas Horn,et al.  The impact of modern-day neuroimaging on the field of deep brain stimulation. , 2019, Current opinion in neurology.

[32]  R. Cameron Craddock,et al.  Detecting stable individual differences in the functional organization of the human basal ganglia , 2017, NeuroImage.

[33]  B. Schlaggar,et al.  Brain structure in pediatric Tourette syndrome , 2016, Molecular Psychiatry.

[34]  Abraham Z. Snyder,et al.  On time delay estimation and sampling error in resting-state fMRI , 2019, NeuroImage.

[35]  T. Videen,et al.  Mapping Go-No-Go performance within the subthalamic nucleus region. , 2010, Brain : a journal of neurology.

[36]  Dustin Scheinost,et al.  The individual functional connectome is unique and stable over months to years , 2017, NeuroImage.

[37]  Michael J. Randazzo,et al.  Network effects of deep brain stimulation. , 2015, Journal of neurophysiology.

[38]  M. Posner,et al.  The attention system of the human brain: 20 years after. , 2012, Annual review of neuroscience.

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

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

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

[42]  P. Strick,et al.  Cingulate Motor Areas , 1993 .

[43]  Clinical review of DBS for Tourette Syndrome. , 2009, Frontiers in bioscience.

[44]  Keith J. Worsley,et al.  The Geometry of Random Images , 1996 .

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

[46]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[47]  Conor Liston,et al.  Atypical Prefrontal Connectivity in Attention-Deficit/Hyperactivity Disorder: Pathway to Disease or Pathological End Point? , 2011, Biological Psychiatry.

[48]  Timothy O. Laumann,et al.  Functional Brain Networks Are Dominated by Stable Group and Individual Factors, Not Cognitive or Daily Variation , 2018, Neuron.

[49]  A. Carvalho,et al.  Deep brain stimulation for treatment-resistant depression: an integrative review of preclinical and clinical findings and translational implications , 2018, Molecular Psychiatry.

[50]  B. Argall,et al.  Simplified intersubject averaging on the cortical surface using SUMA , 2006, Human brain mapping.

[51]  S. Petersen,et al.  Contributions of the pulvinar to visual spatial attention , 1987, Neuropsychologia.

[52]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[53]  M. Walter,et al.  Functional mapping of thalamic nuclei and their integration into cortico-striatal-thalamo-cortical loops via ultra-high resolution imaging—from animal anatomy to in vivo imaging in humans , 2013, Front. Neurosci..

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

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

[56]  J. Mink,et al.  Deep brain stimulation. , 2006, Annual review of neuroscience.

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

[58]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

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

[60]  J. Bogousslavsky,et al.  Thalamic infarcts , 1988, Neurology.

[61]  John L. Bradshaw,et al.  The Neurodevelopmental Frontostriatal Disorders: Evolutionary Adaptiveness and Anomalous Lateralization , 2000, Brain and Language.

[62]  S. Haber,et al.  Estimates of Projection Overlap and Zones of Convergence within Frontal-Striatal Circuits , 2014, The Journal of Neuroscience.

[63]  M E J Newman,et al.  Modularity and community structure in networks. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[66]  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.

[67]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[68]  Suzanne N. Haber,et al.  Corticostriatal circuitry , 2016, Dialogues in clinical neuroscience.

[69]  Jon H Kaas,et al.  Pulvinar and other subcortical connections of dorsolateral visual cortex in monkeys , 2002, The Journal of comparative neurology.

[70]  S. Kühn,et al.  Day2day: investigating daily variability of magnetic resonance imaging measures over half a year , 2017, BMC Neuroscience.

[71]  Philip A Starr,et al.  Microelectrode-guided implantation of deep brain stimulators into the globus pallidus internus for dystonia: techniques, electrode locations, and outcomes. , 2006, Neurosurgical focus.

[72]  Günther Deuschl,et al.  Stimulation site within the MRI‐defined STN predicts postoperative motor outcome , 2012, Movement disorders : official journal of the Movement Disorder Society.

[73]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.

[74]  Nicholas V. Metcalf,et al.  The circuitry of abulia: Insights from functional connectivity MRI , 2014, NeuroImage: Clinical.

[75]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[76]  Suzanne N. Haber,et al.  Convergence of prefrontal and parietal anatomical projections in a connectional hub in the striatum , 2017, NeuroImage.

[77]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[78]  C. Honey,et al.  Hypomania as an adverse effect of subthalamic nucleus stimulation: report of two cases , 2006, Acta Neurochirurgica.

[79]  Maxwell A. Bertolero,et al.  The Human Thalamus Is an Integrative Hub for Functional Brain Networks , 2016, The Journal of Neuroscience.

[80]  Dustin Scheinost,et al.  Influences on the Test–Retest Reliability of Functional Connectivity MRI and its Relationship with Behavioral Utility , 2017, Cerebral cortex.

[81]  S Shipp,et al.  Corticopulvinar connections of areas V5, V4, and V3 in the macaque monkey: A dual model of retinal and cortical topographies , 2001, The Journal of comparative neurology.

[82]  A. Destée,et al.  Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. , 2005, The New England journal of medicine.

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

[84]  S. Grillner,et al.  The evolutionary origin of the vertebrate basal ganglia and its role in action selection , 2013, The Journal of physiology.

[85]  J. Mink Basal ganglia dysfunction in Tourette's syndrome: a new hypothesis. , 2001, Pediatric neurology.

[86]  Evan M. Gordon,et al.  Trait-like variants in human functional brain networks , 2019, Proceedings of the National Academy of Sciences.

[87]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[88]  David Whitney,et al.  Attention gates visual coding in the human pulvinar , 2012, Nature Communications.

[89]  T. Videen,et al.  Mood response to deep brain stimulation of the subthalamic nucleus in Parkinson's disease. , 2012, The Journal of neuropsychiatry and clinical neurosciences.

[90]  J. Ghika,et al.  Subthalamic DBS replaces levodopa in Parkinson’s disease: Two-year follow-up , 2002, Neurology.

[91]  J. Mink The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. , 2003, Archives of neurology.

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

[93]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[94]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.

[95]  H. Ring,et al.  Neuropsychiatry of the basal ganglia , 2002, Journal of neurology, neurosurgery, and psychiatry.

[96]  Evan M. Gordon,et al.  Individual-specific features of brain systems identified with resting state functional correlations , 2017, NeuroImage.

[97]  Y. Agid,et al.  Subthalamic DBS replaces levodopa in Parkinson’s disease: Two-year follow-up , 2003, Neurology.

[98]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[99]  Michael J. Tarr,et al.  Recognizing disguised faces , 2012 .

[100]  Erin K. Molloy,et al.  Using Edge Voxel Information to Improve Motion Regression for rs-fMRI Connectivity Studies , 2015, Brain Connect..

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

[102]  Andreea C. Bostan,et al.  The basal ganglia and the cerebellum: nodes in an integrated network , 2018, Nature Reviews Neuroscience.

[103]  R. Cameron Craddock,et al.  A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics , 2013, NeuroImage.

[104]  Alon Sinai,et al.  Magnetic resonance-guided focused ultrasound thalamotomy for tremor: a report of 30 Parkinson's disease and essential tremor cases. , 2018, Journal of neurosurgery.

[105]  M. C. Campbell,et al.  Neural correlates of STN DBS-induced cognitive variability in Parkinson disease , 2008, Neuropsychologia.

[106]  Joohi Jimenez-Shahed,et al.  The safety and efficacy of thalamic deep brain stimulation in essential tremor: 10 years and beyond , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[107]  S Blond,et al.  Stimulation of the subthalamic nucleus in Parkinson's disease: cognitive and affective changes are not linked to the motor outcome. , 2006, Parkinsonism & related disorders.

[108]  Erik Rietveld,et al.  Clinical Outcome and Mechanisms of Deep Brain Stimulation for Obsessive-Compulsive Disorder , 2015, Current Behavioral Neuroscience Reports.

[109]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[110]  Katherine R. Luking,et al.  Reward Processing and Risk for Depression Across Development , 2016, Trends in Cognitive Sciences.

[111]  Damien A. Fair,et al.  Connectotyping: Model Based Fingerprinting of the Functional Connectome , 2014, PloS one.

[112]  Abraham Z. Snyder,et al.  Maturing Thalamocortical Functional Connectivity Across Development , 2010, Front. Syst. Neurosci..

[113]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[114]  Evan M. Gordon,et al.  Three Distinct Sets of Connector Hubs Integrate Human Brain Function. , 2018, Cell reports.

[115]  R. Buckner,et al.  Resting-state networks link invasive and noninvasive brain stimulation across diverse psychiatric and neurological diseases , 2014, Proceedings of the National Academy of Sciences.

[116]  Yong He,et al.  Graph theoretical modeling of brain connectivity. , 2010, Current opinion in neurology.

[117]  Paul Bentley,et al.  Motor dexterity and strength depend upon integrity of the attention-control system , 2017, Proceedings of the National Academy of Sciences.

[118]  E. G. Jones,et al.  Viewpoint: the core and matrix of thalamic organization , 1998, Neuroscience.

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

[120]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[121]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[122]  R. K. Simpson,et al.  Unilateral thalamic deep brain stimulation for refractory essential tremor and Parkinson's disease tremor , 1998, Neurology.

[123]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[124]  Clémentine Bosch-Bouju,et al.  Motor thalamus integration of cortical, cerebellar and basal ganglia information: implications for normal and parkinsonian conditions , 2013, Front. Comput. Neurosci..

[125]  Carl D. Hacker,et al.  Common Behavioral Clusters and Subcortical Anatomy in Stroke , 2015, Neuron.

[126]  M. Mallar Chakravarty,et al.  The Connectivity of the Human Pulvinar: A Diffusion Tensor Imaging Tractography Study , 2007, Int. J. Biomed. Imaging.

[127]  Timothy S. Coalson,et al.  Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. , 2012, Cerebral cortex.

[128]  Evan M. Gordon,et al.  Spatial and Temporal Organization of the Individual Human Cerebellum , 2018, Neuron.

[129]  Rebecca Treiman,et al.  The English Lexicon Project , 2007, Behavior research methods.

[130]  Michael S. Okun,et al.  Coordinate-Based Lead Location Does Not Predict Parkinson's Disease Deep Brain Stimulation Outcome , 2014, PloS one.

[131]  M. Fox,et al.  Intrinsic functional relations between human cerebral cortex and thalamus. , 2008, Journal of neurophysiology.

[132]  Philip J. Hahn,et al.  Network perspectives on the mechanisms of deep brain stimulation , 2010, Neurobiology of Disease.

[133]  Sabine Kastner,et al.  Visual attention as a multilevel selection process , 2004, Cognitive, affective & behavioral neuroscience.

[134]  Margot J. Taylor,et al.  The centre of the brain: Topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia , 2013, Human brain mapping.

[135]  Marcel van Gerven,et al.  Probabilistic model-based functional parcellation reveals a robust, fine-grained subdivision of the striatum , 2015, NeuroImage.

[136]  Rens Verhagen,et al.  Deep brain stimulation for Parkinson’s disease: defining the optimal location within the subthalamic nucleus , 2018, Journal of Neurology, Neurosurgery, and Psychiatry.

[137]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[138]  Timothy O. Laumann,et al.  Developmental Changes in the Organization of Functional Connections between the Basal Ganglia and Cerebral Cortex , 2014, The Journal of Neuroscience.

[139]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

[140]  Martin Rosvall,et al.  Maps of random walks on complex networks reveal community structure , 2007, Proceedings of the National Academy of Sciences.