Large-scale network interactions supporting item-context memory formation

Episodic memory is thought to involve functional interactions of large-scale brain networks that dynamically reconfigure depending on task demands. Although the hippocampus and closely related structures have been implicated, little is known regarding how large-scale and distributed networks support different memory formation demands. We investigated patterns of interactions among distributed networks while human individuals formed item-context memories for two stimulus categories. Subjects studied object-scene and object-location associations in different fMRI sessions. Stimulus-responsive brain regions were organized based on their fMRI interconnectivity into networks and modules using probabilistic module-detection algorithms to maximize measurement of individual differences in modular structure. Although there was a great deal of consistency in the modular structure between object-scene and object-location memory formation, there were also significant differences. Interactions among functional modules predicted later memory accuracy, explaining substantial portions of variability in memory formation success. Increased interactivity of modules associated with internal thought and anti-correlation of these modules with those related to stimulus-evoked processing robustly predicted object-scene memory, whereas decreased interactivity of stimulus-evoked processing modules predicted object-location memory. Assessment of individual differences in network organization therefore allowed identification of distinct patterns of functional interactions that robustly predicted memory formation. This highlights large-scale brain network interactions for memory formation and indicates that although networks are largely robust to task demands, reconfiguration nonetheless occurs to support distinct memory formation demands.

[1]  Marcia K. Johnson,et al.  Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory? , 2009, Psychological bulletin.

[2]  A. Zalesky,et al.  Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection , 2012, Proceedings of the National Academy of Sciences.

[3]  Jonathan D. Power,et al.  Intrinsic and Task-Evoked Network Architectures of the Human Brain , 2014, Neuron.

[4]  Erik A. Wing,et al.  Hippocampal Contributions to the Large‐Scale Episodic Memory Network Predict Vivid Visual Memories , 2017, Cerebral cortex.

[5]  P. Skudlarski,et al.  Brain Connectivity Related to Working Memory Performance , 2006, The Journal of Neuroscience.

[6]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[7]  Olaf Sporns,et al.  THE HUMAN CONNECTOME: A COMPLEX NETWORK , 2011, Schizophrenia Research.

[8]  John C Gore,et al.  Modulation of steady state functional connectivity in the default mode and working memory networks by cognitive load , 2011, Human brain mapping.

[9]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[10]  Murdock,et al.  The serial position effect of free recall , 1962 .

[11]  Jesse Rissman,et al.  Episodic Memory Retrieval Benefits from a Less Modular Brain Network Organization , 2017, The Journal of Neuroscience.

[12]  M. Corbetta,et al.  Individual variability in functional connectivity predicts performance of a perceptual task , 2012, Proceedings of the National Academy of Sciences.

[13]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[14]  Rachel A. Diana,et al.  Corrigendum: Imaging recollection and familiarity in the medial temporal lobe: a three-component model [ Trends in Cognitive Sciences 11 (2007), 379–386] , 2008, Trends in Cognitive Sciences.

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

[16]  Daniel L. Schacter,et al.  Unitization and grouping mediate dissociations in memory for new , 1989 .

[17]  Joel L. Voss,et al.  Stimulation of the Posterior Cortical-Hippocampal Network Enhances Precision of Memory Recollection , 2017, Current Biology.

[18]  Xi-Nian Zuo,et al.  Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults , 2011, The Journal of Neuroscience.

[19]  Andrew P. Yonelinas,et al.  Functional Connectivity Relationships Predict Similarities in Task Activation and Pattern Information during Associative Memory Encoding , 2014, Journal of Cognitive Neuroscience.

[20]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[21]  Joel L. Voss,et al.  Selective and coherent activity increases due to stimulation indicate functional distinctions between episodic memory networks , 2018, Science Advances.

[22]  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.

[23]  Aude Oliva,et al.  Visual long-term memory has a massive storage capacity for object details , 2008, Proceedings of the National Academy of Sciences.

[24]  James R. Booth,et al.  Changes in Task-Related Functional Connectivity across Multiple Spatial Scales Are Related to Reading Performance , 2013, PloS one.

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

[26]  Tracy H. Wang,et al.  Recollection-Related Increases in Functional Connectivity Predict Individual Differences in Memory Accuracy , 2015, The Journal of Neuroscience.

[27]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[28]  Maureen Ritchey,et al.  Cortico-hippocampal systems involved in memory and cognition: the PMAT framework. , 2015, Progress in brain research.

[29]  Michelle Hampson,et al.  Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. , 2010, Magnetic resonance imaging.

[30]  Danielle S Bassett,et al.  Learning-induced autonomy of sensorimotor systems , 2014, Nature Neuroscience.

[31]  Roberto Cabeza,et al.  Overlapping brain activity between episodic memory encoding and retrieval: Roles of the task-positive and task-negative networks , 2010, NeuroImage.

[32]  P. Skudlarski,et al.  Detection of functional connectivity using temporal correlations in MR images , 2002, Human brain mapping.

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

[34]  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.

[35]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Danielle S. Bassett,et al.  Cognitive Network Neuroscience , 2015, Journal of Cognitive Neuroscience.

[37]  Arne D. Ekstrom,et al.  Multiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans , 2014, Scientific Reports.

[38]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[39]  Olaf Sporns,et al.  Integration and segregation of large-scale brain networks during short-term task automatization , 2016, Nature Communications.

[40]  M E J Newman,et al.  Fast algorithm for detecting community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[42]  Cleofé Peña-Gómez,et al.  Brain connectivity during resting state and subsequent working memory task predicts behavioural performance , 2012, Cortex.

[43]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[44]  Habib Benali,et al.  Partial correlation for functional brain interactivity investigation in functional MRI , 2006, NeuroImage.

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

[46]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[47]  Neal J. Cohen,et al.  The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags , 2006, The Journal of Neuroscience.

[48]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[50]  B T Thomas Yeo,et al.  The modular and integrative functional architecture of the human brain , 2015, Proceedings of the National Academy of Sciences.

[51]  H. Spiers,et al.  Prefrontal and medial temporal lobe interactions in long-term memory , 2003, Nature Reviews Neuroscience.

[52]  Michael D. Rugg,et al.  The Role of the Prefrontal Cortex in Recognition Memory and Memory for Source: An fMRI Study , 1999, NeuroImage.

[53]  Jessica R. Cohen,et al.  The Segregation and Integration of Distinct Brain Networks and Their Relationship to Cognition , 2016, The Journal of Neuroscience.

[54]  Stefan Fürtinger,et al.  Stability of Network Communities as a Function of Task Complexity , 2016, Journal of Cognitive Neuroscience.

[55]  Erik A. Wing,et al.  Neural similarity between encoding and retrieval is related to memory via hippocampal interactions. , 2013, Cerebral cortex.