Reactivation of experience-dependent cell assembly patterns in the hippocampus

The hippocampus is thought to be involved in episodic memory formation by reactivating traces of waking experience during sleep. Indeed, the joint firing of spatially tuned pyramidal cells encoding nearby places recur during sleep. We found that the sleep cofiring of rat CA1 pyramidal cells encoding similar places increased relative to the sleep session before exploration. This cofiring increase depended on the number of times that cells fired together with short latencies (<50 ms) during exploration, and was strongest between cells representing the most visited places. This is indicative of a Hebbian learning rule in which changes in firing associations between cells are determined by the number of waking coincident firing events. In contrast, cells encoding different locations reduced their cofiring in proportion to the number of times that they fired independently. Together these data indicate that reactivated patterns are shaped by both positive and negative changes in cofiring, which are determined by recent behavior.

[1]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

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

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

[4]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[5]  G. Buzsáki Hippocampal sharp waves: Their origin and significance , 1986, Brain Research.

[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]  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.

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

[9]  C. A. Castro,et al.  Recovery of spatial learning deficits after decay of electrically induced synaptic enhancement in the hippocampus , 1989, Nature.

[10]  E. Bostock,et al.  Experience‐dependent modifications of hippocampal place cell firing , 1991, Hippocampus.

[11]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

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

[13]  G. Buzsáki,et al.  Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[15]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  J. Lisman,et al.  Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro , 1995, Neuron.

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

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

[19]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[20]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[21]  R. Morris,et al.  Impaired spatial learning after saturation of long-term potentiation. , 1998, Science.

[22]  J. Csicsvari,et al.  Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus an Ensemble Approach in the Behaving Rat , 1998, Neuron.

[23]  C Kentros,et al.  Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. , 1998, Science.

[24]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

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

[26]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

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

[28]  T. Sejnowski,et al.  Natural patterns of activity and long-term synaptic plasticity , 2000, Current Opinion in Neurobiology.

[29]  J. Csicsvari,et al.  Ensemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events , 2000, Neuron.

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

[31]  R. Morris,et al.  Retrograde Amnesia for Spatial Memory Induced by NMDA Receptor-Mediated Long-Term Potentiation , 2001, The Journal of Neuroscience.

[32]  G. Buzsáki,et al.  Temporal Interaction between Single Spikes and Complex Spike Bursts in Hippocampal Pyramidal Cells , 2001, Neuron.

[33]  J. Csicsvari,et al.  Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  L. Bianchi,et al.  Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats , 2001, Neuroscience.

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

[36]  M. Quirk,et al.  Requirement for Hippocampal CA3 NMDA Receptors in Associative Memory Recall , 2002, Science.

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

[38]  W. K. Cullen,et al.  Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty , 2003, Nature Neuroscience.

[39]  B. McNaughton,et al.  Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. , 2004, Journal of neurophysiology.

[40]  Kenneth D. Harris,et al.  Firing rate modulation: A simple statistical view of memory trace reactivation , 2005, Neural Networks.

[41]  N. Spruston,et al.  Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity , 2005, Nature Neuroscience.

[42]  J. O’Neill,et al.  Place-Selective Firing of CA1 Pyramidal Cells during Sharp Wave/Ripple Network Patterns in Exploratory Behavior , 2006, Neuron.

[43]  Jadin C. Jackson,et al.  Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential Experience , 2006, The Journal of Neuroscience.

[44]  S. Wang,et al.  Malleability of Spike-Timing-Dependent Plasticity at the CA3–CA1 Synapse , 2006, The Journal of Neuroscience.

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

[46]  R. Morris,et al.  Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas , 2006, The European journal of neuroscience.

[47]  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.

[48]  R. K. Simpson Nature Neuroscience , 2022 .