Elaboration Benefits Source Memory Encoding Through Centrality Change

Variations in levels of processing affect memory encoding and subsequent retrieval performance, but it is unknown how processing depth affects communication patterns within the network of interconnected brain regions involved in episodic memory encoding. In 113 healthy adults scanned with functional MRI, we used graph theory to calculate centrality indices representing the brain regions’ relative importance in the memory network. We tested how communication patterns in 42 brain regions involved in episodic memory encoding changed as a function of processing depth, and how these changes were related to episodic memory ability. Centrality changes in right middle frontal gyrus, right inferior parietal lobule and left superior frontal gyrus were positively related to semantic elaboration during encoding. In the same regions, centrality during successful episodic memory encoding was related to performance on the episodic memory task, indicating that these centrality changes reflect processes that support memory encoding through deep elaborative processing. Similar analyses were performed for congruent trials, i.e. events that fit into existing knowledge structures, but no relationship between centrality changes and congruity were found. The results demonstrate that while elaboration and congruity have similar beneficial effects on source memory performance, the cortical signatures of these processes are probably not identical.

[1]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[2]  H. Walter,et al.  The relationship between level of processing and hippocampal–cortical functional connectivity during episodic memory formation in humans , 2013, Human brain mapping.

[3]  Y. Stern,et al.  Source Memory and Encoding Strategy in Normal Aging , 2000, Journal of clinical and experimental neuropsychology.

[4]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[5]  Markus H. Sneve,et al.  Mechanisms Underlying Encoding of Short-Lived Versus Durable Episodic Memories , 2015, The Journal of Neuroscience.

[6]  D. Head,et al.  Neuroanatomical and cognitive mediators of age-related differences in episodic memory. , 2008, Neuropsychology.

[7]  C. Madan,et al.  Making Memories That Last , 2015, The Journal of Neuroscience.

[8]  Guillén Fernández,et al.  Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans , 2010, Proceedings of the National Academy of Sciences.

[9]  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.

[10]  P. Bonacich TECHNIQUE FOR ANALYZING OVERLAPPING MEMBERSHIPS , 1972 .

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

[12]  A. Schulman Memory for words recently classified , 1974, Memory & cognition.

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

[14]  R. Buckner,et al.  Neural correlates of verbal memory encoding during semantic and structural processing tasks , 2001, Neuroreport.

[15]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[16]  Anat Maril,et al.  Event congruency and episodic encoding: A developmental fMRI study , 2011, Neuropsychologia.

[17]  G. Galli What Makes Deeply Encoded Items Memorable? Insights into the Levels of Processing Framework from Neuroimaging and Neuromodulation , 2014, Front. Psychiatry.

[18]  Klaus Lehnertz,et al.  Identifying important nodes in weighted functional brain networks: a comparison of different centrality approaches. , 2012, Chaos.

[19]  A. M. Dale,et al.  A hybrid approach to the skull stripping problem in MRI , 2004, NeuroImage.

[20]  J. C. Gray,et al.  Event congruency enhances episodic memory encoding through semantic elaboration and relational binding. , 2009, Cerebral cortex.

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

[22]  L. Freeman Centrality in social networks conceptual clarification , 1978 .

[23]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[24]  J. Pillai Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[25]  Benjamin R. Geib,et al.  From hippocampus to whole‐brain: The role of integrative processing in episodic memory retrieval , 2017, Human brain mapping.

[26]  Anders M. Dale,et al.  Sequence-independent segmentation of magnetic resonance images , 2004, NeuroImage.

[27]  Hongkeun Kim,et al.  Differential neural activity in the recognition of old versus new events: An Activation Likelihood Estimation Meta‐Analysis , 2013, Human brain mapping.

[28]  John T. Serences,et al.  A comparison of methods for characterizing the event-related BOLD timeseries in rapid fMRI , 2004, NeuroImage.

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

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

[31]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[32]  K. Paller,et al.  Observing the transformation of experience into memory , 2002, Trends in Cognitive Sciences.

[33]  Bruce Fischl,et al.  Highly accurate inverse consistent registration: A robust approach , 2010, NeuroImage.

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

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

[36]  Cyma Van Petten,et al.  Prefrontal Engagement during Source Memory Retrieval Depends on the Prior Encoding Task , 2006, Journal of Cognitive Neuroscience.

[37]  P. Johnson-Laird,et al.  Meaning, amount of processing, and memory for words , 1978 .

[38]  Arthur P. Shimamura,et al.  Episodic retrieval and the cortical binding of relational activity , 2011, Cognitive, affective & behavioral neuroscience.

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

[40]  Edward T. Bullmore,et al.  Connectomic Intermediate Phenotypes for Psychiatric Disorders , 2012, Front. Psychiatry.

[41]  F. Craik,et al.  Levels of processing: A framework for memory research , 1972 .

[42]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[43]  R N Henson,et al.  Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. , 2001, Brain : a journal of neurology.

[44]  Cynthia M. Lakon,et al.  How Correlated Are Network Centrality Measures? , 2008, Connections.

[45]  Yonatan Goshen-Gottstein,et al.  Delineating the Effect of Semantic Congruency on Episodic Memory: The Role of Integration and Relatedness , 2015, PloS one.

[46]  Craig J. Brozinsky,et al.  Functional connectivity with the hippocampus during successful memory formation , 2005, Hippocampus.

[47]  L. Davachi Item, context and relational episodic encoding in humans , 2006, Current Opinion in Neurobiology.

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

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

[50]  O. Sporns,et al.  Identification and Classification of Hubs in Brain Networks , 2007, PloS one.

[51]  C. Grady,et al.  Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation , 2009, Neuropsychologia.

[52]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[53]  Lars Nyberg,et al.  Levels of processing: A view from functional brain imaging , 2002, Memory.

[54]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

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

[56]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[57]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI I. The Method , 2001, NeuroImage.

[58]  F. Craik,et al.  Depth of processing and the retention of words , 1975 .

[59]  Paul C. Fletcher,et al.  Regional Brain Activations Predicting Subsequent Memory Success: An Event-Related Fmri Study of the Influence of Encoding Tasks , 2003, Cortex.

[60]  F. Craik Levels of processing: Past, present... and future? , 2002, Memory.

[61]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[62]  F. Craik,et al.  Levels of Pro-cessing: A Framework for Memory Research , 1975 .

[63]  Hongkeun Kim,et al.  Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies , 2011, NeuroImage.

[64]  L. Nadel,et al.  Memory consolidation, retrograde amnesia and the hippocampal complex , 1997, Current Opinion in Neurobiology.

[65]  J. Raaijmakers,et al.  Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. , 2003, Brain : a journal of neurology.

[66]  S. Wasserman,et al.  Social Network Analysis: List of Illustrations , 1994 .

[67]  Stanley Wasserman,et al.  Social Network Analysis: Methods and Applications , 1994 .