Dorsoventral and Proximodistal Hippocampal Processing Account for the Influences of Sleep and Context on Memory (Re)consolidation: A Connectionist Model

The context in which learning occurs is sufficient to reconsolidate stored memories and neuronal reactivation may be crucial to memory consolidation during sleep. The mechanisms of context-dependent and sleep-dependent memory (re)consolidation are unknown but involve the hippocampus. We simulated memory (re)consolidation using a connectionist model of the hippocampus that explicitly accounted for its dorsoventral organization and for CA1 proximodistal processing. Replicating human and rodent (re)consolidation studies yielded the following results. (1) Semantic overlap between memory items and extraneous learning was necessary to explain experimental data and depended crucially on the recurrent networks of dorsal but not ventral CA3. (2) Stimulus-free, sleep-induced internal reactivations of memory patterns produced heterogeneous recruitment of memory items and protected memories from subsequent interference. These simulations further suggested that the decrease in memory resilience when subjects were not allowed to sleep following learning was primarily due to extraneous learning. (3) Partial exposure to the learning context during simulated sleep (i.e., targeted memory reactivation) uniformly increased memory item reactivation and enhanced subsequent recall. Altogether, these results show that the dorsoventral and proximodistal organization of the hippocampus may be important components of the neural mechanisms for context-based and sleep-based memory (re)consolidations.

[1]  A. Hupbach,et al.  The dynamics of memory: context-dependent updating. , 2008, Learning & memory.

[2]  W. Gan,et al.  REM sleep selectively prunes and maintains new synapses in development and learning , 2017, Nature Neuroscience.

[3]  M. Moser,et al.  Representation of Geometric Borders in the Entorhinal Cortex , 2008, Science.

[4]  Patrick Verga,et al.  Modeling Reconsolidation in Kernel Associative Memory , 2013, PloS one.

[5]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[6]  J. Born,et al.  Sleep enhances false memories depending on general memory performance , 2010, Behavioural Brain Research.

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

[8]  I. Wilhelm,et al.  Prior knowledge is essential for the beneficial effect of targeted memory reactivation during sleep , 2017, Scientific Reports.

[9]  E. Moser,et al.  Spatial representation and the architecture of the entorhinal cortex , 2006, Trends in Neurosciences.

[10]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[11]  Jean-Marc Fellous,et al.  Remaking memories: reconsolidation updates positively motivated spatial memory in rats. , 2012, Learning & memory.

[12]  Edmund T Rolls,et al.  An attractor network in the hippocampus: theory and neurophysiology. , 2007, Learning & memory.

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

[14]  W. Gan,et al.  Sleep promotes branch-specific formation of dendritic spines after learning , 2014, Science.

[15]  Sachin S. Deshmukh,et al.  Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local–global reference frames , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[16]  C. Barnes,et al.  Spatial Representation along the Proximodistal Axis of CA1 , 2010, Neuron.

[17]  S. Ribeiro,et al.  Brain gene expression during REM sleep depends on prior waking experience. , 1999, Learning & memory.

[18]  W. Gerstner,et al.  Synaptic Consolidation: From Synapses to Behavioral Modeling , 2015, The Journal of Neuroscience.

[19]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

[20]  R. O’Reilly Six principles for biologically based computational models of cortical cognition , 1998, Trends in Cognitive Sciences.

[21]  Howard Eichenbaum,et al.  Ventral Hippocampal Neurons Are Shaped by Experience to Represent Behaviorally Relevant Contexts , 2013, The Journal of Neuroscience.

[22]  Joel L. Voss,et al.  Memory reactivation and consolidation during sleep. , 2004, Learning & memory (Cold Spring Harbor, N.Y.).

[23]  G. Tononi,et al.  Sleep-Dependent Synaptic Down-Selection (I): Modeling the Benefits of Sleep on Memory Consolidation and Integration , 2013, Front. Neurol..

[24]  Randall C. O'Reilly,et al.  Biologically Plausible Error-Driven Learning Using Local Activation Differences: The Generalized Recirculation Algorithm , 1996, Neural Computation.

[25]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[26]  Vadym Gnatkovsky,et al.  Hippocampus-Mediated Activation of Superficial and Deep Layer Neurons in the Medial Entorhinal Cortex of the Isolated Guinea Pig Brain , 2006, The Journal of Neuroscience.

[27]  Jonathan L. C. Lee Reconsolidation: maintaining memory relevance , 2009, Trends in Neurosciences.

[28]  H. Eichenbaum,et al.  Robust Conjunctive Item–Place Coding by Hippocampal Neurons Parallels Learning What Happens Where , 2009, The Journal of Neuroscience.

[29]  E. Rolls,et al.  A computational theory of hippocampal function, and tests of the theory: New developments , 2015, Neuroscience & Biobehavioral Reviews.

[30]  Brian Mingus,et al.  The Emergent neural modeling system , 2008, Neural Networks.

[31]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[32]  F. H. Lopes da Silva,et al.  Two reentrant pathways in the hippocampal‐entorhinal system , 2004, Hippocampus.

[33]  R. Kesner Behavioral functions of the CA3 subregion of the hippocampus. , 2007, Learning & memory.

[34]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[35]  S. Ribeiro,et al.  Induction of Hippocampal Long-Term Potentiation during Waking Leads to Increased Extrahippocampal zif-268 Expression during Ensuing Rapid-Eye-Movement Sleep , 2002, The Journal of Neuroscience.

[36]  F. H. Lopes da Silva,et al.  Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re‐entrance in the hippocampal–entorhinal system , 2003, The European journal of neuroscience.

[37]  A. Hupbach,et al.  Reconsolidation of episodic memories: a subtle reminder triggers integration of new information. , 2007, Learning & memory.

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

[39]  Michael C. Anderson Rethinking interference theory: Executive control and the mechanisms of forgetting. , 2003 .

[40]  Martin Llofriu,et al.  Goal-oriented robot navigation learning using a multi-scale space representation , 2015, Neural Networks.

[41]  L. Nadel Dorsal and ventral hippocampal lesions and behavior , 1968 .

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

[43]  Matthijs A. A. van der Meer,et al.  Hippocampal Replay Is Not a Simple Function of Experience , 2010, Neuron.

[44]  Ken A Paller,et al.  The Benefits of Targeted Memory Reactivation for Consolidation in Sleep are Contingent on Memory Accuracy and Direct Cue-Memory Associations. , 2016, Sleep.

[45]  JaneR . Taylor,et al.  Molecular mechanisms of memory reconsolidation , 2007, Nature Reviews Neuroscience.

[46]  James J. Knierim,et al.  CA3 Retrieves Coherent Representations from Degraded Input: Direct Evidence for CA3 Pattern Completion and Dentate Gyrus Pattern Separation , 2014, Neuron.

[47]  Giulio Tononi,et al.  Sleep and Synaptic Homeostasis: Structural Evidence in Drosophila , 2011, Science.

[48]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[49]  David N. Lyttle,et al.  Spatial scale and place field stability in a grid‐to‐place cell model of the dorsoventral axis of the hippocampus , 2013, Hippocampus.

[50]  J. Born,et al.  Odor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation , 2007, Science.

[51]  James J Knierim,et al.  Lateral entorhinal neurons are not spatially selective in cue‐rich environments , 2011, Hippocampus.

[52]  Daniel Johnston,et al.  Mapping the electrophysiological and morphological properties of CA1 pyramidal neurons along the longitudinal hippocampal axis , 2016, Hippocampus.

[53]  Brian J. Wiltgen,et al.  Memory retrieval along the proximodistal axis of CA1 , 2016, Hippocampus.

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

[55]  F. Louzada,et al.  State of the art on targeted memory reactivation: Sleep your way to enhanced cognition. , 2017, Sleep medicine reviews.

[56]  Sidarta Ribeiro,et al.  Synaptic Homeostasis and Restructuring across the Sleep-Wake Cycle , 2015, PLoS Comput. Biol..

[57]  R. Llinás,et al.  Role of the hippocampal-entorhinal loop in temporal lobe epilepsy: extra- and intracellular study in the isolated guinea pig brain in vitro , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  B. McNaughton,et al.  Modeling the spontaneous reactivation of experience‐specific hippocampal cell assembles during sleep , 1996, Hippocampus.

[59]  R. Kesner,et al.  The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat , 2005, Hippocampus.

[60]  G. Tononi,et al.  Sleep function and synaptic homeostasis. , 2006, Sleep medicine reviews.

[61]  Jonathan L. C. Lee,et al.  Memory reconsolidation mediates the strengthening of memories by additional learning , 2008, Nature Neuroscience.

[62]  Serge Laroche,et al.  Reconsolidation of memory: A decade of debate , 2012, Progress in Neurobiology.

[63]  Keith B. Hengen,et al.  Firing Rate Homeostasis in Visual Cortex of Freely Behaving Rodents , 2013, Neuron.

[64]  A. Hupbach,et al.  Memory formation, consolidation and transformation , 2012, Neuroscience & Biobehavioral Reviews.

[65]  P. Frankland,et al.  Finding the engram , 2015, Nature Reviews Neuroscience.

[66]  Bruce McNaughton,et al.  Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience , 1998, Journal of sleep research.

[67]  Jean-Marc Fellous,et al.  Contextual reminders fail to trigger memory reconsolidation in aged rats and aged humans , 2015, Neurobiology of Learning and Memory.

[68]  T. Engen,et al.  Odor memory: Review and analysis , 1996, Psychonomic bulletin & review.

[69]  C. Degueldre,et al.  Are Spatial Memories Strengthened in the Human Hippocampus during Slow Wave Sleep? , 2004, Neuron.

[70]  Justin C. Hulbert,et al.  Interfering with Theories of Sleep and Memory: Sleep, Declarative Memory, and Associative Interference , 2006, Current Biology.

[71]  Michael D. Howard,et al.  Complementary Learning Systems , 2014, Cogn. Sci..

[72]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

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

[74]  Pierre Lavenex,et al.  Building hippocampal circuits to learn and remember: Insights into the development of human memory , 2013, Behavioural Brain Research.

[75]  Maxim Bazhenov,et al.  Hippocampal CA1 Ripples as Inhibitory Transients , 2016, PLoS Comput. Biol..

[76]  M. Avoli,et al.  CA3-Driven Hippocampal-Entorhinal Loop Controls Rather than Sustains In Vitro Limbic Seizures , 1997, The Journal of Neuroscience.

[77]  K. Nader,et al.  Memory reconsolidation: an update , 2010, Annals of the New York Academy of Sciences.

[78]  Jean-Marc Fellous,et al.  Hippocampal Anatomy Supports the Use of Context in Object Recognition: A Computational Model , 2013, Comput. Intell. Neurosci..

[79]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[80]  Jessica D. Payne,et al.  The role of sleep in declarative memory consolidation: passive, permissive, active or none? , 2006, Current Opinion in Neurobiology.

[81]  Sean M. Polyn,et al.  Human memory reconsolidation can be explained using the temporal context model , 2011, Psychonomic bulletin & review.

[82]  K. Paller,et al.  Upgrading the sleeping brain with targeted memory reactivation , 2013, Trends in Cognitive Sciences.

[83]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[84]  G. Tononi,et al.  Sleep and synaptic homeostasis: a hypothesis , 2003, Brain Research Bulletin.

[85]  H. Eichenbaum Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.