High-fidelity mapping of repetition-related changes in the parietal memory network

fMRI studies of human memory have identified a "parietal memory network" (PMN) that displays distinct responses to novel and familiar stimuli, typically deactivating during initial encoding but robustly activating during retrieval. The small size of PMN regions, combined with their proximity to the neighboring default mode network, makes a targeted assessment of their responses in highly sampled subjects important for understanding information processing within the network. Here, we describe an experiment in which participants made semantic decisions about repeatedly-presented stimuli, assessing PMN BOLD responses as items transitioned from experimentally novel to repeated. Data are from the highly-sampled subjects in the Midnight Scan Club dataset, enabling a characterization of BOLD responses at both the group and single-subject level. Across all analyses, PMN regions deactivated in response to novel stimuli and displayed changes in BOLD activity across presentations, but did not significantly activate to repeated items. Results support only a portion of initially hypothesized effects, in particular suggesting that novelty-related deactivations may be less susceptible to attentional/task manipulations than are repetition-related activations within the network. This in turn suggests that novelty and familiarity may be processed as separable entities within the PMN.

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

[2]  Abraham Z. Snyder,et al.  CHAPTER 26 – Difference Image vs Ratio Image Error Function Forms in PET—PET Realignment , 1996 .

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

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

[5]  Stefan Glasauer,et al.  Rapid and independent memory formation in the parietal cortex , 2016, Proceedings of the National Academy of Sciences.

[6]  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.

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

[8]  Kathryn J. Devaney,et al.  Cortical and Subcortical Contributions to Long-Term Memory-Guided Visuospatial Attention , 2018, Cerebral cortex.

[9]  Jeffrey G. Ojemann,et al.  The parietal memory network activates similarly for true and associative false recognition elicited via the DRM procedure , 2017, Cortex.

[10]  Jonathan D. Power,et al.  Studying Brain Organization via Spontaneous fMRI Signal , 2014, Neuron.

[11]  Sanghoon Han,et al.  The Inferior Parietal Lobule and Recognition Memory: Expectancy Violation or Successful Retrieval? , 2010, The Journal of Neuroscience.

[12]  Arthur P. Shimamura,et al.  Task relevance modulates successful retrieval effects during explicit and implicit memory tests , 2011, NeuroImage.

[13]  D. Schacter,et al.  Priming and the Brain , 1998, Neuron.

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

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

[16]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

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

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

[19]  Ingrid R. Olson,et al.  Some surprising findings on the involvement of the parietal lobe in human memory , 2009, Neurobiology of Learning and Memory.

[20]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  Evan M. Gordon,et al.  On the Stability of BOLD fMRI Correlations , 2016, Cerebral cortex.

[22]  Adrian W. Gilmore,et al.  Neural Signatures of Test-Potentiated Learning in Parietal Cortex , 2013, The Journal of Neuroscience.

[23]  Gagan S. Wig,et al.  The Critical Roles of Localization and Physiology for Understanding Parietal Contributions to Memory Retrieval , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[24]  M. Rugg,et al.  Ventral lateral parietal cortex and episodic memory retrieval , 2017, Cortex.

[25]  Karl K. Szpunar,et al.  Laboratory-based and autobiographical retrieval tasks differ substantially in their neural substrates , 2009, Neuropsychologia.

[26]  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.

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

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

[29]  Catie Chang,et al.  Connectivity trajectory across lifespan differentiates the precuneus from the default network , 2014, NeuroImage.

[30]  Morris Moscovitch,et al.  Response to Nelson et al.: ventral parietal subdivisions are not incompatible with an overarching function , 2012, Trends in Cognitive Sciences.

[31]  Daniel L. Schacter,et al.  Specificity of priming: a cognitive neuroscience perspective , 2004, Nature Reviews Neuroscience.

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

[33]  R. Sperling,et al.  What goes down must come up: role of the posteromedial cortices in encoding and retrieval. , 2011, Cerebral cortex.

[34]  Rama Chellappa,et al.  Recognizing Disguised Faces in the Wild , 2018, IEEE Transactions on Biometrics, Behavior, and Identity Science.

[35]  Steven E. Petersen,et al.  Separable responses to error, ambiguity, and reaction time in cingulo-opercular task control regions , 2014, NeuroImage.

[36]  Steven E. Petersen,et al.  In favor of a ‘fractionation’ view of ventral parietal cortex: comment on Cabeza et al. , 2012, Trends in Cognitive Sciences.

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

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

[39]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[40]  Oluwasanmi Koyejo,et al.  Toward open sharing of task-based fMRI data: the OpenfMRI project , 2013, Front. Neuroinform..

[41]  J. Mugler,et al.  Three‐dimensional magnetization‐prepared rapid gradient‐echo imaging (3D MP RAGE) , 1990, Magnetic resonance in medicine.

[42]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[43]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[44]  Maurizio Corbetta,et al.  The contribution of the human posterior parietal cortex to episodic memory , 2017, Nature Reviews Neuroscience.

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

[46]  Curt Burgess,et al.  Producing high-dimensional semantic spaces from lexical co-occurrence , 1996 .

[47]  M. Moscovitch,et al.  Top-down and bottom-up attention to memory: A hypothesis (AtoM) on the role of the posterior parietal cortex in memory retrieval , 2008, Neuropsychologia.

[48]  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.

[49]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[50]  D. Schacter,et al.  Cortical activity reductions during repetition priming can result from rapid response learning , 2004, Nature.

[51]  Patrick S. R. Davidson,et al.  Does lateral parietal cortex support episodic memory? Evidence from focal lesion patients , 2008, Neuropsychologia.

[52]  David C Somers,et al.  Cognitive Control Network Contributions to Memory-Guided Visual Attention. , 2016, Cerebral cortex.

[53]  Roberto Cabeza,et al.  Parietal Lobe and Episodic Memory: Bilateral Damage Causes Impaired Free Recall of Autobiographical Memory , 2007, The Journal of Neuroscience.

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

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

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

[57]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[58]  Libor Spacek,et al.  Distinctive Descriptions for Face Processing , 1997, BMVC.

[59]  R L Buckner,et al.  Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Nader Pouratian,et al.  Single-Neuron Representation of Memory Strength and Recognition Confidence in Left Human Posterior Parietal Cortex , 2018, Neuron.

[61]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[62]  Michael Wilson,et al.  MRC psycholinguistic database: Machine-usable dictionary, version 2.00 , 1988 .

[63]  R. Cabeza,et al.  Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. , 2006, Journal of neurophysiology.

[64]  Risto Miikkulainen,et al.  Behavioral, neuroimaging, and computational evidence for perceptual caching in repetition priming , 2010, Brain Research.

[65]  U. Rutishauser,et al.  Representation of retrieval confidence by single neurons in the human medial temporal lobe , 2015, Nature Neuroscience.

[66]  I. Dobbins,et al.  Unexpected novelty and familiarity orienting responses in lateral parietal cortex during recognition judgment , 2013, Neuropsychologia.

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

[68]  Reisa A. Sperling,et al.  The Encoding/Retrieval Flip: Interactions between Memory Performance and Memory Stage and Relationship to Intrinsic Cortical Networks , 2013, Journal of Cognitive Neuroscience.

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

[70]  Nachum Soroker,et al.  Parietal lesion effects on cued recall following pair associate learning , 2015, Neuropsychologia.

[71]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

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

[73]  Alex Martin,et al.  Neural correlates of semantic and episodic memory retrieval , 1998, Neuropsychologia.

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

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

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

[77]  Marian E. Berryhill,et al.  Insights from neuropsychology: pinpointing the role of the posterior parietal cortex in episodic and working memory , 2012, Front. Integr. Neurosci..

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

[79]  Ed Vul,et al.  Voodoo and circularity errors , 2012, NeuroImage.

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

[81]  Carson C. Chow,et al.  Repetition priming and repetition suppression: A case for enhanced efficiency through neural synchronization , 2012, Cognitive neuroscience.

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

[83]  Sau-chin Chen,et al.  Creating false memories: Remembering words not presented in lists. , 2018 .

[84]  Gagan S. Wig,et al.  Retrieval The Critical Roles of Localization and Physiology for Understanding Parietal Contributions to Memory , 2013 .

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

[86]  Jane E Herron,et al.  Probability effects on the neural correlates of retrieval success: an fMRI study , 2004, NeuroImage.

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

[88]  Hongkeun Kim,et al.  Brain regions that show repetition suppression and enhancement: A meta‐analysis of 137 neuroimaging experiments , 2017, Human brain mapping.

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

[90]  R. Buckner,et al.  Cluster size thresholds for assessment of significant activation in fMRI , 2001, NeuroImage.

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

[92]  M. Seghier The Angular Gyrus , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[93]  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.

[94]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[95]  Bentin Shlomo Neural correlates of semantic and episodic memory for faces: evidence from multiple frequency bands , 2008 .

[96]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[97]  Randy L. Buckner,et al.  Set-and Code-Specific Activation in the Frontal Cortex: An fMRI Study of Encoding and Retrieval of Faces and Words , 1999, Journal of Cognitive Neuroscience.

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

[99]  Kaia L. Vilberg,et al.  Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective , 2008, Neuropsychologia.

[100]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

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