Parallel hippocampal-parietal circuits for self- and goal-oriented processing

Significance The finding that human hippocampal-cortical functional connectivity is nonunitary, separated along functional network borders (default mode network [DMN], self-oriented; parietal memory network [PMN], goal-oriented) in the anterior–posterior axis, raises various possibilities as to why this organization might be beneficial and could inform updates to current models of human hippocampal function, memory, and the self. The hippocampus is critically important for a diverse range of cognitive processes, such as episodic memory, prospective memory, affective processing, and spatial navigation. Using individual-specific precision functional mapping of resting-state functional MRI data, we found the anterior hippocampus (head and body) to be preferentially functionally connected to the default mode network (DMN), as expected. The hippocampal tail, however, was strongly preferentially functionally connected to the parietal memory network (PMN), which supports goal-oriented cognition and stimulus recognition. This anterior–posterior dichotomy of resting-state functional connectivity was well-matched by differences in task deactivations and anatomical segmentations of the hippocampus. Task deactivations were localized to the hippocampal head and body (DMN), relatively sparing the tail (PMN). The functional dichotomization of the hippocampus into anterior DMN-connected and posterior PMN-connected parcels suggests parallel but distinct circuits between the hippocampus and medial parietal cortex for self- versus goal-oriented processing.

[1]  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.

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

[3]  Evan M. Gordon,et al.  Plasticity and Spontaneous Activity Pulses in Disused Human Brain Circuits , 2020, Neuron.

[4]  Adrian W. Gilmore,et al.  A parietal memory network revealed by multiple MRI methods , 2015, Trends in Cognitive Sciences.

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

[6]  Christian F. Doeller,et al.  Memory hierarchies map onto the hippocampal long axis in humans , 2015, Nature Neuroscience.

[7]  Evan M. Gordon,et al.  Integrative and Network-Specific Connectivity of the Basal Ganglia and Thalamus Defined in Individuals , 2019, Neuron.

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

[9]  Mohit H. Adhikari,et al.  Hippocampal Sharp-Wave Ripples Influence Selective Activation of the Default Mode Network , 2016, Current Biology.

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

[11]  Anthony R. McIntosh,et al.  Memory encoding and hippocampally-based novelty/familiarity discrimination networks , 2003, Neuropsychologia.

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

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

[14]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

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

[16]  Brian A. Gordon,et al.  Effects of aging and Alzheimer's disease along the longitudinal axis of the hippocampus. , 2013, Journal of Alzheimer's disease : JAD.

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

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

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

[20]  R. Buckner,et al.  Parcellating Cortical Functional Networks in Individuals , 2015, Nature Neuroscience.

[21]  C. Liston,et al.  Branched Photoswitchable Tethered Ligands Enable Ultra-efficient Optical Control and Detection of G Protein-Coupled Receptors In Vivo , 2019, Neuron.

[22]  Yong Hu,et al.  Brain resting-state functional MRI connectivity: Morphological foundation and plasticity , 2014, NeuroImage.

[23]  Ole Paulsen,et al.  Hippocampal network oscillations — recent insights from in vitro experiments , 2015, Current Opinion in Neurobiology.

[24]  Andrew P. Yonelinas,et al.  Detecting Changes in Scenes: The Hippocampus Is Critical for Strength-Based Perception , 2013, Neuron.

[25]  G. Buzsáki,et al.  Traveling Theta Waves along the Entire Septotemporal Axis of the Hippocampus , 2012, Neuron.

[26]  Rodrigo M. Braga,et al.  The detailed organization of the human cerebellum estimated by intrinsic functional connectivity within the individual , 2020, bioRxiv.

[27]  E. Lein,et al.  Functional organization of the hippocampal longitudinal axis , 2014, Nature Reviews Neuroscience.

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

[29]  Jürgen R. Reichenbach,et al.  Resting state functional connectivity of the hippocampus along the anterior–posterior axis and its association with glutamatergic metabolism , 2016, Cortex.

[30]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

[31]  György Buzsáki,et al.  Space and time in the brain , 2017, Science.

[32]  남동석,et al.  III , 1751, Olav Audunssøn.

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

[34]  Ana M. Daugherty,et al.  A reliable and valid method for manual demarcation of hippocampal head, body, and tail , 2015, International Journal of Developmental Neuroscience.

[35]  Alexandros Kafkas,et al.  Two separate, but interacting, neural systems for familiarity and novelty detection: A dual‐route mechanism , 2014, Hippocampus.

[36]  H. Eichenbaum,et al.  Interplay of Hippocampus and Prefrontal Cortex in Memory , 2013, Current Biology.

[37]  R. A. Cooper,et al.  Deconstructing the Posterior Medial Episodic Network , 2020, Trends in Cognitive Sciences.

[38]  Bert Sakmann,et al.  Spontaneous persistent activity in entorhinal cortex modulates cortico-hippocampal interaction in vivo , 2012, Nature Neuroscience.

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

[40]  Itamar Kahn,et al.  The Organization of Mouse and Human Cortico-Hippocampal Networks Estimated by Intrinsic Functional Connectivity , 2016, Cerebral cortex.

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

[42]  C. Ranganath,et al.  Two cortical systems for memory-guided behaviour , 2012, Nature Reviews Neuroscience.

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

[44]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: III. Cortical efferents , 2003, The Journal of comparative neurology.

[45]  Beatriz Luna,et al.  The role of experience in adolescent cognitive development: Integration of executive, memory, and mesolimbic systems , 2016, Neuroscience & Biobehavioral Reviews.

[46]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

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

[48]  Evan M. Gordon,et al.  Individual-specific functional connectivity of the amygdala: A substrate for precision psychiatry , 2020, Proceedings of the National Academy of Sciences.

[49]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

[50]  M. Raichle,et al.  Human cortical–hippocampal dialogue in wake and slow-wave sleep , 2016, Proceedings of the National Academy of Sciences.

[51]  P. Matthews,et al.  Hippocampal Neuroinflammation, Functional Connectivity, and Depressive Symptoms in Multiple Sclerosis , 2016, Biological Psychiatry.

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

[53]  M. Raichle,et al.  Correction for Li et al., Functional connectivity arises from a slow rhythmic mechanism , 2015, Proceedings of the National Academy of Sciences.

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

[55]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[56]  A. Grace,et al.  Dopamine modulation of hippocampal-prefrontal cortical interaction drives memory-guided behavior. , 2008, Cerebral cortex.

[57]  Arne D. Ekstrom,et al.  Differential Connectivity of Perirhinal and Parahippocampal Cortices within Human Hippocampal Subregions Revealed by High-Resolution Functional Imaging , 2012, The Journal of Neuroscience.

[58]  Evan M. Gordon,et al.  Human Fronto-Striatal Connectivity is Organized into Discrete Functional Subnetworks , 2021, bioRxiv.

[59]  F Andermann,et al.  Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging , 1992, Neurology.

[60]  Morris Moscovitch,et al.  Multiple Scales of Representation along the Hippocampal Anteroposterior Axis in Humans , 2018, Current Biology.

[61]  Evan M. Gordon,et al.  High-fidelity mapping of repetition-related changes in the parietal memory network , 2019, NeuroImage.

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

[63]  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.

[64]  Ryan V. Raut,et al.  Hierarchical dynamics as a macroscopic organizing principle of the human brain , 2020, Proceedings of the National Academy of Sciences.

[65]  T. Hafting,et al.  Finite Scale of Spatial Representation in the Hippocampus , 2008, Science.

[66]  M. Greicius,et al.  Default-Mode Activity during a Passive Sensory Task: Uncoupled from Deactivation but Impacting Activation , 2004, Journal of Cognitive Neuroscience.

[67]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[68]  Alexandra T. Keinath,et al.  Precise spatial coding is preserved along the longitudinal hippocampal axis , 2014, Hippocampus.

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

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

[71]  Koene R. A. Van Dijk,et al.  The parahippocampal gyrus links the default‐mode cortical network with the medial temporal lobe memory system , 2014, Human brain mapping.

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

[73]  Adrian W. Gilmore,et al.  The Contextual Association Network Activates More for Remembered than for Imagined Events. , 2014, Cerebral cortex.

[74]  G. V. Van Hoesen,et al.  Neural connections of the posteromedial cortex in the macaque , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[77]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[78]  L. Luo,et al.  Deep posteromedial cortical rhythm in dissociation , 2020, Nature.

[79]  Morris Moscovitch,et al.  The hippocampus and related neocortical structures in memory transformation , 2018, Neuroscience Letters.

[80]  Daniela Montaldi,et al.  How do memory systems detect and respond to novelty? , 2018, Neuroscience Letters.

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

[82]  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.

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

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

[85]  Gary F. Egan,et al.  Optimizing Hippocampal Segmentation in Infants Utilizing MRI Post-Acquisition Processing , 2011, Neuroinformatics.

[86]  M. Bar Visual objects in context , 2004, Nature Reviews Neuroscience.

[87]  M. Rajadhyaksha,et al.  Confocal imaging-guided laser ablation of basal cell carcinomas: an ex vivo study. , 2015, The Journal of investigative dermatology.

[88]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[89]  Lawrence H Snyder,et al.  Functional connectivity arises from a slow rhythmic mechanism , 2015, Proceedings of the National Academy of Sciences.

[90]  Arne D. Ekstrom,et al.  Space, Time and Episodic Memory: the Hippocampus is all over the Cognitive Map , 2017, bioRxiv.

[91]  G. Buzsáki,et al.  Space and Time: The Hippocampus as a Sequence Generator , 2018, Trends in Cognitive Sciences.

[92]  H. Duvernoy,et al.  The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI , 1997 .

[93]  Justin L. Vincent,et al.  Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[94]  Hallvard Røe Evensmoen,et al.  Long-axis specialization of the human hippocampus , 2013, Trends in Cognitive Sciences.

[95]  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.

[96]  Sean M Montgomery,et al.  Integration and Segregation of Activity in Entorhinal-Hippocampal Subregions by Neocortical Slow Oscillations , 2006, Neuron.

[97]  L. Swanson,et al.  Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex , 2007, Brain Research Reviews.

[98]  Margaret L. Schlichting,et al.  Learning-related representational changes reveal dissociable integration and separation signatures in the hippocampus and prefrontal cortex , 2015, Nature Communications.

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

[100]  Charan Ranganath,et al.  Dynamic Cortico-hippocampal Networks Underlying Memory and Cognition: The PMAT Framework , 2017 .

[101]  Jonathan D. Power,et al.  A Parcellation Scheme for Human Left Lateral Parietal Cortex , 2010, Neuron.

[102]  M. Weiner,et al.  Reduced hippocampal functional connectivity in Alzheimer disease. , 2007, Archives of neurology.

[103]  Reinder Vos de Wael,et al.  Anatomical and microstructural determinants of hippocampal subfield functional connectome embedding , 2018, Proceedings of the National Academy of Sciences.

[104]  Arne D. Ekstrom,et al.  Space, time, and episodic memory: The hippocampus is all over the cognitive map , 2018, Hippocampus.

[105]  Evan M. Gordon,et al.  Cingulo-Opercular Control Network Supports Disused Motor Circuits in Standby Mode , 2020, bioRxiv.

[106]  Chunshui Yu,et al.  Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia , 2008, Schizophrenia Research.

[107]  Ali R. Khan,et al.  Diffusion MRI of the Unfolded Hippocampus , 2020, bioRxiv.

[108]  Stephen J. Gotts,et al.  Identifying task-general effects of stimulus familiarity in the parietal memory network , 2019, Neuropsychologia.

[109]  Adrian W. Gilmore,et al.  Are There Multiple Kinds of Episodic Memory? An fMRI Investigation Comparing Autobiographical and Recognition Memory Tasks , 2017, The Journal of Neuroscience.

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

[111]  Deborah E. Hannula,et al.  The Hippocampus from Cells to Systems , 2017 .

[112]  Evan M. Gordon,et al.  Default-mode network streams for coupling to language and control systems , 2020, Proceedings of the National Academy of Sciences.

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