Sharp wave ripples during learning stabilize hippocampal spatial map

Cognitive representation of the environment requires a stable hippocampal map, but the mechanisms maintaining a given map are unknown. Because sharp wave-ripples (SPW-R) orchestrate both retrospective and prospective spatial information, we hypothesized that disrupting neuronal activity during SPW-Rs affects spatial representation. Mice learned new sets of three goal locations daily in a multiwell maze. We used closed-loop SPW-R detection at goal locations to trigger optogenetic silencing of a subset of CA1 pyramidal neurons. Control place cells (nonsilenced or silenced outside SPW-Rs) largely maintained the location of their place fields after learning and showed increased spatial information content. In contrast, the place fields of SPW-R-silenced place cells remapped, and their spatial information remained unaltered. SPW-R silencing did not impact the firing rates or proportions of place cells. These results suggest that interference with SPW-R-associated activity during learning prevents stabilization and refinement of hippocampal maps.

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

[2]  Brad E. Pfeiffer,et al.  Hippocampal place cell sequences depict future paths to remembered goals , 2013, Nature.

[3]  E. Tolman.  Cognitive maps in rats and men. , 1948, Psychological review.

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

[5]  Fraser T. Sparks,et al.  Neuronal code for extended time in the hippocampus , 2012, Proceedings of the National Academy of Sciences.

[6]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[8]  B. McNaughton,et al.  Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input , 1994, Hippocampus.

[9]  H. Eichenbaum,et al.  Consolidation and Reconsolidation: Two Lives of Memories? , 2011, Neuron.

[10]  RU Muller,et al.  The hippocampus as a cognitive graph , 1996, The Journal of general physiology.

[11]  Lynn Hazan,et al.  Klusters, NeuroScope, NDManager: A free software suite for neurophysiological data processing and visualization , 2006, Journal of Neuroscience Methods.

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

[13]  G. Buzsáki,et al.  Dendritic Spikes Are Enhanced by Cooperative Network Activity in the Intact Hippocampus , 1998, The Journal of Neuroscience.

[14]  Jozsef Csicsvari,et al.  Activity-dependent plasticity of hippocampal place maps , 2016, Nature Communications.

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

[16]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[17]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

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

[19]  B. McNaughton,et al.  Memory trace reactivation in hippocampal and neocortical neuronal ensembles , 2000, Current Opinion in Neurobiology.

[20]  Jozsef Csicsvari,et al.  Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus , 2016, PloS one.

[21]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[22]  David J. Anderson,et al.  Subregion- and Cell Type–Restricted Gene Knockout in Mouse Brain , 1996, Cell.

[23]  D. Dupret,et al.  Recoding a cocaine-place memory engram to a neutral engram in the hippocampus , 2016, Nature Neuroscience.

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

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

[26]  Eran Stark,et al.  Local generation of multineuronal spike sequences in the hippocampal CA1 region , 2015, Proceedings of the National Academy of Sciences.

[27]  G. Buzsáki,et al.  Inhibition-Induced Theta Resonance in Cortical Circuits , 2013, Neuron.

[28]  E. Kandel,et al.  Increased Attention to Spatial Context Increases Both Place Field Stability and Spatial Memory , 2004, Neuron.

[29]  S. Arber,et al.  A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling , 2005, PLoS biology.

[30]  Bruce L. McNaughton,et al.  Progressive Transformation of Hippocampal Neuronal Representations in “Morphed” Environments , 2005, Neuron.

[31]  Jozsef Csicsvari,et al.  Dynamic Reconfiguration of Hippocampal Interneuron Circuits during Spatial Learning , 2013, Neuron.

[32]  Kamran Diba,et al.  Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons , 2012, Hippocampus.

[33]  J. O’Neill,et al.  Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration , 2007, The European journal of neuroscience.

[34]  G. Buzsáki,et al.  Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations , 2014, Neuron.

[35]  G. Buzsáki.  Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning , 2015, Hippocampus.

[36]  R. Kesner,et al.  Role of parietal cortex and hippocampus in representing spatial information. , 1991, Cerebral cortex.

[37]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[38]  Nace L. Golding,et al.  Dendritic spikes as a mechanism for cooperative long-term potentiation , 2002, Nature.

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

[40]  Joseph D. Monaco,et al.  Attentive Scanning Behavior Drives One-Trial Potentiation of Hippocampal Place Fields , 2014, Nature Neuroscience.

[41]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[42]  Shantanu P. Jadhav,et al.  Interplay between Hippocampal Sharp-Wave-Ripple Events and Vicarious Trial and Error Behaviors in Decision Making , 2016, Neuron.

[43]  Susumu Tonegawa,et al.  Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons , 2015, Nature Neuroscience.

[44]  G. Ascoli,et al.  A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval. , 2005, Learning & memory.

[45]  J. Knierim,et al.  Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3 , 2004, Nature.

[46]  Margaret F. Carr,et al.  Hippocampal SWR Activity Predicts Correct Decisions during the Initial Learning of an Alternation Task , 2013, Neuron.

[47]  Eran Stark,et al.  Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. , 2012, Journal of neurophysiology.

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

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

[50]  J. O’Neill,et al.  The reorganization and reactivation of hippocampal maps predict spatial memory performance , 2010, Nature Neuroscience.

[51]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[52]  Michael A. Henninger,et al.  High-Performance Genetically Targetable Optical Neural Silencing via Light-Driven Proton Pumps , 2010 .

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

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

[55]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[56]  Caleb Kemere,et al.  Rapid and Continuous Modulation of Hippocampal Network State during Exploration of New Places , 2013, PloS one.

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

[58]  Allan R. Jones,et al.  A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing , 2012, Nature Neuroscience.

[59]  Joseph E LeDoux,et al.  Reply — reconsolidation: The labile nature of consolidation theory , 2000, Nature Reviews Neuroscience.

[60]  D. Johnston,et al.  Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. , 1998, Annual review of physiology.

[61]  L. Frank,et al.  New Experiences Enhance Coordinated Neural Activity in the Hippocampus , 2008, Neuron.

[62]  B. McNaughton,et al.  Experience-dependent, asymmetric expansion of hippocampal place fields. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[64]  M. Wilson,et al.  VTA neurons coordinate with the hippocampal reactivation of spatial experience , 2015, eLife.