Deciphering Neural Codes of Memory during Sleep

Memories of experiences are stored in the cerebral cortex. Sleep is critical for the consolidation of hippocampal memory of wake experiences into the neocortex. Understanding representations of neural codes of hippocampal-neocortical networks during sleep would reveal important circuit mechanisms in memory consolidation and provide novel insights into memory and dreams. Although sleep-associated ensemble spike activity has been investigated, identifying the content of memory in sleep remains challenging. Here we revisit important experimental findings on sleep-associated memory (i.e., neural activity patterns in sleep that reflect memory processing) and review computational approaches to the analysis of sleep-associated neural codes (SANCs). We focus on two analysis paradigms for sleep-associated memory and propose a new unsupervised learning framework ('memory first, meaning later') for unbiased assessment of SANCs.

[1]  G Buzsáki,et al.  Memory consolidation during sleep: a neurophysiological perspective. , 1998, Journal of sleep research.

[2]  A. Oeltermann,et al.  Hippocampal–cortical interaction during periods of subcortical silence , 2012, Nature.

[3]  G. Tononi,et al.  Local sleep in awake rats , 2011, Nature.

[4]  Isabel C. Hutchison,et al.  The role of REM sleep theta activity in emotional memory , 2015, Front. Psychol..

[5]  S. Tonegawa,et al.  Creating a False Memory in the Hippocampus , 2013, Science.

[6]  D. R. Euston,et al.  Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep , 2007, Science.

[7]  L. Colgin Rhythms of the hippocampal network , 2016, Nature Reviews Neuroscience.

[8]  Rosa Cossart,et al.  Awake hippocampal reactivations project onto orthogonal neuronal assemblies , 2016, Science.

[9]  M. Wilson,et al.  Uncovering representations of sleep-associated hippocampal ensemble spike activity , 2016, Scientific Reports.

[10]  B. McNaughton,et al.  Preferential Reactivation of Motivationally Relevant Information in the Ventral Striatum , 2008, The Journal of Neuroscience.

[11]  Matthew A Wilson,et al.  Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus , 2014, eLife.

[12]  Rosa Cossart,et al.  Internally Recurring Hippocampal Sequences as a Population Template of Spatiotemporal Information , 2015, Neuron.

[13]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[14]  R. Quiroga,et al.  Extracting information from neuronal populations : information theory and decoding approaches , 2022 .

[15]  Matthew A. Wilson,et al.  Neural Representation of Spatial Topology in the Rodent Hippocampus , 2013, Neural Computation.

[16]  B L McNaughton,et al.  Coordinated Reactivation of Distributed Memory Traces in Primate Neocortex , 2002, Science.

[17]  M. Khamassi,et al.  Replay of rule-learning related neural patterns in the prefrontal cortex during sleep , 2009, Nature Neuroscience.

[18]  Elizabeth A. Kensinger,et al.  Sleep’s Role in the Consolidation of Emotional Episodic Memories , 2010 .

[19]  B L McNaughton,et al.  Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. , 1998, Journal of neurophysiology.

[20]  S. Corkin What's new with the amnesic patient H.M.? , 2002, Nature Reviews Neuroscience.

[21]  J. Csicsvari,et al.  Communication between neocortex and hippocampus during sleep in rodents , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  E N Brown,et al.  A Statistical Paradigm for Neural Spike Train Decoding Applied to Position Prediction from Ensemble Firing Patterns of Rat Hippocampal Place Cells , 1998, The Journal of Neuroscience.

[23]  B. McNaughton,et al.  Replay of Neuronal Firing Sequences in Rat Hippocampus During Sleep Following Spatial Experience , 1996, Science.

[24]  R. Morris,et al.  Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. , 2010, Annual review of psychology.

[25]  Susumu Takahashi Hierarchical organization of context in the hippocampal episodic code , 2013, eLife.

[26]  B. McNaughton,et al.  Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions. , 2004, Learning & memory.

[27]  R. Stickgold Sleep-dependent memory consolidation , 2005, Nature.

[28]  E. Loftus Planting misinformation in the human mind: a 30-year investigation of the malleability of memory. , 2005, Learning & memory.

[29]  J. Born,et al.  The contribution of sleep to hippocampus-dependent memory consolidation , 2007, Trends in Cognitive Sciences.

[30]  Robert E. Hampson,et al.  Distribution of spatial and nonspatial information in dorsal hippocampus , 1999, Nature.

[31]  Lacey J. Kitch,et al.  Long-term dynamics of CA1 hippocampal place codes , 2013, Nature Neuroscience.

[32]  Daniel Levenstein,et al.  Network Homeostasis and State Dynamics of Neocortical Sleep , 2016, Neuron.

[33]  S. Jego,et al.  Optogenetic identification of a rapid-eye-movement (REM) sleep modulatory circuit in the hypothalamus , 2013, Nature Neuroscience.

[34]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[35]  B. McNaughton,et al.  Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics , 1999, The Journal of Neuroscience.

[36]  Manuel Schabus,et al.  Spontaneous neural activity during human slow wave sleep , 2008, Proceedings of the National Academy of Sciences.

[37]  J. Csicsvari,et al.  Replay and Time Compression of Recurring Spike Sequences in the Hippocampus , 1999, The Journal of Neuroscience.

[38]  Tobias Holzhammer,et al.  Integration of silicon-based neural probes and micro-drive arrays for chronic recording of large populations of neurons in behaving animals , 2016, Journal of neural engineering.

[39]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[40]  Elad Eban,et al.  A cortical–hippocampal–cortical loop of information processing during memory consolidation , 2016, Nature Neuroscience.

[41]  Matthew A. Wilson,et al.  Uncovering spatial topology represented by rat hippocampal population neuronal codes , 2012, Journal of Computational Neuroscience.

[42]  J. Born,et al.  About sleep's role in memory. , 2013, Physiological reviews.

[43]  J. Born,et al.  Sleep inspires insight , 2004, Nature.

[44]  D. Margoliash,et al.  Song replay during sleep and computational rules for sensorimotor vocal learning. , 2000, Science.

[45]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[46]  Matthew A Wilson,et al.  A combinatorial method for analyzing sequential firing patterns involving an arbitrary number of neurons based on relative time order. , 2004, Journal of neurophysiology.

[47]  Francis Crick,et al.  The function of dream sleep , 1983, Nature.

[48]  K. Ganguly,et al.  Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation , 2015, PLoS biology.

[49]  R. Velluti,et al.  Interactions between sleep and sensory physiology , 1997, Journal of sleep research.

[50]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[51]  G. Buzsáki,et al.  The log-dynamic brain: how skewed distributions affect network operations , 2014, Nature Reviews Neuroscience.

[52]  Y Kamitani,et al.  Neural Decoding of Visual Imagery During Sleep , 2013, Science.

[53]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[54]  Yang Dan,et al.  Circuit-based interrogation of sleep control , 2016, Nature.

[55]  Caswell Barry,et al.  Coordinated grid and place cell replay during rest , 2016, Nature Neuroscience.

[56]  Matthew A. Wilson,et al.  Hippocampal Replay of Extended Experience , 2009, Neuron.

[57]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[58]  Kenneth D Harris,et al.  Sleep replay meets brain–machine interface , 2014, Nature Neuroscience.

[59]  Liam Paninski,et al.  Inferring synaptic inputs given a noisy voltage trace via sequential Monte Carlo methods , 2012, Journal of Computational Neuroscience.

[60]  Jan Born,et al.  Sleep-Stage-Specific Regulation of Cortical Excitation and Inhibition , 2016, Current Biology.

[61]  J. Born,et al.  The memory function of sleep , 2010, Nature Reviews Neuroscience.

[62]  Demetris K. Roumis,et al.  Hippocampal sharp-wave ripples in waking and sleeping states , 2015, Current Opinion in Neurobiology.

[63]  Antoine Adamantidis,et al.  Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation , 2016, Science.

[64]  Eran Stark,et al.  Large-scale, high-density (up to 512 channels) recording of local circuits in behaving animals. , 2014, Journal of neurophysiology.

[65]  Michael L. Roukes,et al.  Nanofabricated Neural Probes for Dense 3-D Recordings of Brain Activity , 2016, Nano letters.

[66]  M. Lavine,et al.  Long-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas , 2004, PLoS biology.

[67]  Andres D. Grosmark,et al.  Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences , 2016, Science.

[68]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[69]  E. Pastalkova,et al.  Clique topology reveals intrinsic geometric structure in neural correlations , 2015, Proceedings of the National Academy of Sciences.

[70]  K. Deisseroth,et al.  Optogenetic stimulation of a hippocampal engram activates fear memory recall , 2012, Nature.

[71]  David J. Foster,et al.  Reverse replay of behavioural sequences in hippocampal place cells during the awake state , 2006, Nature.

[72]  Yaniv Ziv,et al.  Hippocampal ensemble dynamics timestamp events in long-term memory , 2015, eLife.

[73]  M. Wilson,et al.  Optogenetic activation of cholinergic neurons in the PPT or LDT induces REM sleep , 2014, Proceedings of the National Academy of Sciences.

[74]  Sarah J. Cohen,et al.  The Rodent Hippocampus Is Essential for Nonspatial Object Memory , 2013, Current Biology.

[75]  L. Frank,et al.  Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory , 2012, Science.

[76]  M. Tanter,et al.  Local hippocampal fast gamma rhythms precede brain-wide hyperemic patterns during spontaneous rodent REM sleep , 2018, Nature Communications.

[77]  Mathieu Wolff,et al.  Beyond Spatial Memory: The Anterior Thalamus and Memory for the Temporal Order of a Sequence of Odor Cues , 2006, The Journal of Neuroscience.

[78]  Milos R. Popovic,et al.  Closed-Loop Interruption of Hippocampal Ripples through Fornix Stimulation in the Non-Human Primate , 2016, Brain Stimulation.

[79]  Carina Curto,et al.  What can topology tell us about the neural code , 2016, 1605.01905.

[80]  M. H. What ’ s new with the amnesic patient , 2022 .

[81]  Kevin Q Shan,et al.  Spatial tuning and brain state account for dorsal hippocampal CA1 activity in a non-spatial learning task , 2016, eLife.

[82]  J. Born,et al.  Boosting slow oscillations during sleep potentiates memory , 2006, Nature.

[83]  T. Bliss,et al.  The Hippocampus Book , 2006 .

[84]  Bruce L. McNaughton,et al.  Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep , 2000, Brain Research.

[85]  B. Staresina,et al.  Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep , 2015, Nature Neuroscience.

[86]  C. Pavlides,et al.  Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  M. Zugaro,et al.  Hippocampo-cortical coupling mediates memory consolidation during sleep , 2016, Nature Neuroscience.

[88]  Joel L. Voss,et al.  Strengthening Individual Memories by Reactivating Them During Sleep , 2009, Science.

[89]  Mehdi Khamassi,et al.  Principal component analysis of ensemble recordings reveals cell assemblies at high temporal resolution , 2009, Journal of Computational Neuroscience.

[90]  R. Vertes,et al.  Memory Consolidation in Sleep Dream or Reality , 2004, Neuron.

[91]  I. Fried,et al.  Regional Slow Waves and Spindles in Human Sleep , 2011, Neuron.

[92]  Yuri Dabaghian,et al.  Reconceiving the hippocampal map as a topological template , 2014, eLife.

[93]  David Wood,et al.  Luddites must not block progress in genetics , 1999, Nature.

[94]  Karim Benchenane,et al.  Explicit memory creation during sleep demonstrates a causal role of place cells in navigation , 2015, Nature Neuroscience.

[95]  D. Ji,et al.  Initiation of sleep-dependent cortical-hippocampal correlations at wakefulness-sleep transition. , 2014, Journal of neurophysiology.

[96]  Charlotte N. Boccara,et al.  Superficial layers of the medial entorhinal cortex replay independently of the hippocampus , 2017, Science.

[97]  G. Buzsáki,et al.  REM Sleep Reorganizes Hippocampal Excitability , 2012, Neuron.

[98]  G. Dragoi,et al.  Preplay of future place cell sequences by hippocampal cellular assemblies , 2011, Nature.

[99]  J. Knierim The hippocampus , 2015, Current Biology.

[100]  M. Wilson,et al.  Temporally Structured Replay of Awake Hippocampal Ensemble Activity during Rapid Eye Movement Sleep , 2001, Neuron.

[101]  N. Fortin,et al.  Nonspatial Sequence Coding in CA1 Neurons , 2016, The Journal of Neuroscience.

[102]  L. Fuentemilla,et al.  Hippocampus-Dependent Strengthening of Targeted Memories via Reactivation during Sleep in Humans , 2013, Current Biology.

[103]  B. McNaughton,et al.  The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples , 2004, The Journal of Neuroscience.

[104]  K. Ganguly,et al.  Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning , 2014, Nature Neuroscience.

[105]  Yao Lu,et al.  Wireless Neurosensor for Full-Spectrum Electrophysiology Recordings during Free Behavior , 2014, Neuron.

[106]  S. Tonegawa,et al.  Memory Engram Cells Have Come of Age , 2015, Neuron.

[107]  Konrad P Kording,et al.  How advances in neural recording affect data analysis , 2011, Nature Neuroscience.

[108]  B. McNaughton,et al.  Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[109]  G. Tononi,et al.  Cortical Firing and Sleep Homeostasis , 2009, Neuron.

[110]  S. Tonegawa,et al.  Bidirectional switch of the valence associated with a hippocampal contextual memory engram , 2014, Nature.

[111]  Matthew A. Wilson,et al.  A Bayesian nonparametric approach for uncovering rat hippocampal population codes during spatial navigation , 2016, Journal of Neuroscience Methods.

[112]  Jerome M. Siegel,et al.  The REM Sleep-Memory Consolidation Hypothesis , 2001, Science.

[113]  Mayank R. Mehta,et al.  Multisensory Control of Hippocampal Spatiotemporal Selectivity , 2013, Science.

[114]  G. Buzsáki,et al.  Forward and reverse hippocampal place-cell sequences during ripples , 2007, Nature Neuroscience.

[115]  D. Dupret,et al.  Hippocampal Offline Reactivation Consolidates Recently Formed Cell Assembly Patterns during Sharp Wave-Ripples , 2016, Neuron.

[116]  J. Born,et al.  Auditory Closed-Loop Stimulation of the Sleep Slow Oscillation Enhances Memory , 2013, Neuron.

[117]  John A. King,et al.  How vision and movement combine in the hippocampal place code , 2012, Proceedings of the National Academy of Sciences.

[118]  E. Robertson,et al.  Memory Processing: The Critical Role of Neuronal Replay during Sleep , 2013, Current Biology.

[119]  Vítor Lopes-dos-Santos,et al.  Detecting cell assemblies in large neuronal populations , 2013, Journal of Neuroscience Methods.

[120]  F. Mauguière,et al.  Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans , 2010, Proceedings of the National Academy of Sciences.

[121]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[122]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[123]  Daniel Bendor,et al.  Biasing the content of hippocampal replay during sleep , 2012, Nature Neuroscience.

[124]  Giulio Tononi,et al.  Single-neuron activity and eye movements during human REM sleep and awake vision , 2015, Nature Communications.

[125]  D. Cai,et al.  REM, not incubation, improves creativity by priming associative networks , 2009, Proceedings of the National Academy of Sciences.