Probing the neural dynamics of mnemonic representations in humans

Memories are not stored as static engrams, but as dynamic representations affected by processes occurring after initial encoding. Previous studies revealed changes in activity and mnemonic representations in visual processing areas, parietal lobe, and hippocampus underlying repeated retrieval and suppression. However, these neural changes are usually induced by memory modulation immediately after memory formation. Here, we investigated 27 healthy participants with a two-day functional Magnetic Resonance Imaging design to probe how established memories are dynamically modulated by retrieval and suppression 24 hours after learning. Behaviorally, we demonstrated that established memories can still be strengthened by repeated retrieval. By contrast, repeated suppression had a modest negative effect, and suppression-induced forgetting was associated with individual suppression efficacy. Neurally, we demonstrated item-specific pattern reinstatements in visual processing areas, parietal lobe, and hippocampus. Then, we showed that repeated retrieval reduced activity amplitude in the ventral visual cortex and hippocampus, but enhanced the distinctiveness of activity patterns in the ventral visual cortex and parietal lobe. Critically, reduced activity was associated with enhanced representation of idiosyncratic memory traces in ventral visual cortex and precuneus. In contrast, repeated memory suppression was associated with the reduced lateral prefrontal activity, but relative intact mnemonic representations. Our results replicated most of the neural changes induced by memory retrieval and suppression immediately after learning and extended those findings to established memories after initial consolidation. Active retrieval seems to promote episode-unique mnemonic representations in the neocortex after initial encoding but also consolidation. Highlights Repeated retrieval strengthened consolidated memories, while repeated suppression had a modest negative effect. Pattern reinstatements of individual memories were detected in the visual area, parietal lobe, and hippocampus after 24 hours. After repeated retrieval, reduced activity amplitude was associated with increased distinctiveness of activity patterns in the ventral visual cortex and right precuneus. Repeated suppression was associated with the reduced lateral prefrontal activity, but unchanged mnemonic representations.

[1]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[2]  Zara M. Bergström,et al.  The University of Birmingham ( Live System ) Neural markers of inhibition in human memory retrieval , 2016 .

[3]  Kai Li,et al.  Computational approaches to fMRI analysis , 2017, Nature Neuroscience.

[4]  Michael C. Anderson,et al.  Adaptive Top–Down Suppression of Hippocampal Activity and the Purging of Intrusive Memories from Consciousness , 2015, Journal of Cognitive Neuroscience.

[5]  D. Shohamy,et al.  Integrating Memories in the Human Brain: Hippocampal-Midbrain Encoding of Overlapping Events , 2008, Neuron.

[6]  S. Kosslyn,et al.  Neural Systems Shared by Visual Imagery and Visual Perception: A Positron Emission Tomography Study , 1997, NeuroImage.

[7]  Jeffrey D. Karpicke,et al.  The Critical Importance of Retrieval for Learning , 2008, Science.

[8]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[10]  F. D. Lange,et al.  How Do Expectations Shape Perception? , 2018, Trends in Cognitive Sciences.

[11]  Catarina S. Ferreira,et al.  Retrieval as a Fast Route to Memory Consolidation , 2017, Trends in Cognitive Sciences.

[12]  Christian F. Doeller,et al.  Reinstatement of Associative Memories in Early Visual Cortex Is Signaled by the Hippocampus , 2014, The Journal of Neuroscience.

[13]  Yuan Chang Leong,et al.  Shared memories reveal shared structure in neural activity across individuals , 2016, Nature Neuroscience.

[14]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[15]  Guillén Fernández,et al.  Shift from Hippocampal to Neocortical Centered Retrieval Network with Consolidation , 2009, The Journal of Neuroscience.

[16]  M Wimber,et al.  Prefrontal dopamine and the dynamic control of human long-term memory , 2011, Translational Psychiatry.

[17]  Erik A. Wing,et al.  Neural correlates of retrieval-based memory enhancement: An fMRI study of the testing effect , 2013, Neuropsychologia.

[18]  Michael C. Anderson,et al.  Suppressing unwanted memories by executive control , 2001, Nature.

[19]  Michael C. Anderson,et al.  Successfully controlling intrusive memories is harder when control must be sustained , 2017, Memory.

[20]  E. Steegers,et al.  Validation of the Dutch Short Form of the State Scale of the Spielberger State-Trait Anxiety Inventory: Considerations for Usage in Screening Outcomes , 2003, Public Health Genomics.

[21]  N. Kanwisher,et al.  Mental Imagery of Faces and Places Activates Corresponding Stimulus-Specific Brain Regions , 2000, Journal of Cognitive Neuroscience.

[22]  Alberto Llera,et al.  ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data , 2015, NeuroImage.

[23]  Michael C. Anderson,et al.  Tracking the intrusion of unwanted memories into awareness with event-related potentials , 2016, Neuropsychologia.

[24]  Michael C. Anderson,et al.  Purging of Memories from Conscious Awareness Tracked in the Human Brain , 2012, The Journal of Neuroscience.

[25]  C S Ferreira,et al.  Retrieval aids the creation of a generalised memory trace and strengthens episode-unique information , 2019, NeuroImage.

[26]  T. Curran,et al.  Prefrontal Regions Orchestrate Suppression of Emotional Memories via a Two-Phase Process , 2007, Science.

[27]  P. Lang.  International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

[28]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[29]  A. Beck,et al.  Norms for the Beck Depression Inventory (BDI-II) in a Large Dutch Community Sample , 2013 .

[30]  Ninon Burgos,et al.  New advances in the Clinica software platform for clinical neuroimaging studies , 2019 .

[31]  Bert Jonsson,et al.  Lesser Neural Pattern Similarity across Repeated Tests Is Associated with Better Long-Term Memory Retention , 2015, The Journal of Neuroscience.

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

[33]  Jim M. Monti,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[34]  Lars Nyberg,et al.  Rewiring the brain with repeated retrieval: A parametric fMRI study of the testing effect , 2011, Neuroscience Letters.

[35]  P. Frankland,et al.  The organization of recent and remote memories , 2005, Nature Reviews Neuroscience.

[36]  Yuejia Luo,et al.  Memory consolidation reconfigures neural pathways involved in the suppression of emotional memories , 2016, Nature Communications.

[37]  Russell A. Poldrack,et al.  Analyses of regional-average activation and multivoxel pattern information tell complementary stories , 2012, Neuropsychologia.

[38]  Vaidehi S. Natu,et al.  Category-Specific Cortical Activity Precedes Retrieval During Memory Search , 2005, Science.

[39]  Guillén Fernández,et al.  Neural correlates of testing effects in vocabulary learning , 2013, NeuroImage.

[40]  Michael J. Constantino,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008 .

[41]  C. Summerfield,et al.  Expectation in perceptual decision making: neural and computational mechanisms , 2014, Nature Reviews Neuroscience.

[42]  Michael C. Anderson,et al.  Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression , 2015, Nature Neuroscience.

[43]  M. Jenkinson.  Non-linear registration aka Spatial normalisation , 2007 .

[44]  Michael C. Anderson,et al.  Suppressing unwanted memories reduces their unconscious influence via targeted cortical inhibition , 2014, Proceedings of the National Academy of Sciences.

[45]  Eliane Segers,et al.  Neurocognitive mechanisms of the “testing effect”: A review , 2016, Trends in Neuroscience and Education.

[46]  H. Ebbinghaus.  Über das Gedächtniss: Untersuchungen zur experimentellen Psychologie , 1885 .

[47]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

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

[49]  Manuel Schabus,et al.  Rehearsal initiates systems memory consolidation, sleep makes it last , 2019, Science Advances.

[50]  B. McNaughton,et al.  Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Dwight J Kravitz,et al.  Differential Representations of Perceived and Retrieved Visual Information in Hippocampus and Cortex. , 2018, Cerebral cortex.

[52]  Michael C. Anderson,et al.  Neural mechanisms of motivated forgetting , 2014, Trends in Cognitive Sciences.

[53]  Janneke F. M. Jehee,et al.  Less Is More: Expectation Sharpens Representations in the Primary Visual Cortex , 2012, Neuron.

[54]  Url PubMed.  Retrieval Practice Produces More Learning than Elaborative Studying with Concept Mapping , 2012 .

[55]  John T. Serences,et al.  Coexisting representations of sensory and mnemonic information in human visual cortex , 2019, Nature Neuroscience.

[56]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Daniel J Buysse,et al.  The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research , 1989, Psychiatry Research.

[58]  Ali R. Khan,et al.  FreeSurfer-initiated fully-automated subcortical brain segmentation in MRI using Large Deformation Diffeomorphic Metric Mapping , 2008, NeuroImage.

[59]  Gui Xue,et al.  Transformed Neural Pattern Reinstatement during Episodic Memory Retrieval , 2017, The Journal of Neuroscience.

[60]  Henry L. Roediger,et al.  Repeated retrieval during learning is the key to long-term retention , 2007 .

[61]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[62]  Alexander Borst,et al.  How does Nature Program Neuron Types? , 2008, Front. Neurosci..

[63]  Ayanna K. Thomas,et al.  Retrieval practice protects memory against acute stress , 2016, Science.

[64]  Matthias S. Treder,et al.  Evidence that neural information flow is reversed between object perception and object reconstruction from memory , 2018, Nature Communications.

[65]  G. Müller,et al.  Experimentelle Beiträge zur Lehre vom Gedächtniss , 1900 .

[66]  Brice A. Kuhl,et al.  Lower Parietal Encoding Activation Is Associated with Sharper Information and Better Memory , 2016, Cerebral cortex.

[67]  Brice A. Kuhl,et al.  Resistance to forgetting associated with hippocampus-mediated reactivation during new learning , 2010, Nature Neuroscience.

[68]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[69]  Michael C. Anderson,et al.  Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories , 2017, The Journal of Neuroscience.

[70]  R. F. Thompson,et al.  The search for the engram. , 1976, The American psychologist.

[71]  C. Smyth,et al.  The Pittsburgh Sleep Quality Index. , 2003, Dermatology nursing.

[72]  Michael C. Anderson,et al.  A supramodal role of the basal ganglia in memory and motor inhibition: Meta-analytic evidence , 2018, Neuropsychologia.

[73]  Brice A. Kuhl,et al.  Neural Systems Underlying the Suppression of Unwanted Memories , 2004, Science.

[74]  Maureen Ritchey,et al.  Neural reactivation in parietal cortex enhances memory for episodically linked information , 2018, Proceedings of the National Academy of Sciences.

[75]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[76]  Gui Xue,et al.  The Neural Representations Underlying Human Episodic Memory , 2018, Trends in Cognitive Sciences.

[77]  Jeffrey D. Karpicke,et al.  Retrieval Practice Produces More Learning than Elaborative Studying with Concept Mapping , 2011, Science.