Sequence Reactivation in the Hippocampus Is Impaired in Aged Rats

The hippocampus is thought to coordinate memory consolidation by reactivating traces from behavioral experience when the brain is not actively processing new input. In fact, during slow-wave sleep, the patterns of CA1 pyramidal cell ensemble activity correlations are reactivated in both young and aged rats. In addition to correlated activity patterns, repetitive track running also creates a recurring sequence of pyramidal cell activity. The present study compared CA1 sequence activity pattern replay in young and old animals during rest periods after behavior. Whereas the young rats exhibited significant sequence reactivation, it was markedly impaired in the aged animals. When the spatial memory scores of all animals were compared with the degree of sequence reactivation, there was a significant correlation. The novel finding that weak replay of temporal patterns has behavioral consequences, strengthens the idea that reactivation processes are integral to memory consolidation.

[1]  Henry Schmitz,et al.  Congenital Hemolytic Anemias , 1942 .

[2]  James L Olds,et al.  Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. , 1954, Journal of comparative and physiological psychology.

[3]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[4]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  J. B. Ranck,et al.  Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats , 1975, Experimental Neurology.

[6]  J. D. McGaugh,et al.  Impaired synaptic potentiation processes in the hippocampus of aged, memory-deficient rats , 1978, Brain Research.

[7]  C. Barnes.  Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. , 1979, Journal of comparative and physiological psychology.

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

[9]  Bruce L. McNaughton,et al.  The stereotrode: A new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records , 1983, Journal of Neuroscience Methods.

[10]  Fred H. Gage,et al.  Spatial learning and motor deficits in aged rats , 1984, Neurobiology of Aging.

[11]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

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

[13]  P. E. Gold,et al.  Sleep and memory relationships in intact old and amnestic young rats , 1988, Neurobiology of Aging.

[14]  D. Olton,et al.  Individual differences in aging: Behavioral and neurobiological correlates , 1989, Neurobiology of Aging.

[15]  L. Squire,et al.  The primate hippocampal formation: evidence for a time-limited role in memory storage. , 1990, Science.

[16]  G. Winocur.  Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions , 1990, Behavioural Brain Research.

[17]  Bruce L. McNaughton,et al.  An Information-Theoretic Approach to Deciphering the Hippocampal Code , 1992, NIPS.

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

[19]  B. McNaughton,et al.  Region‐specific age effects on AMPA sensitivity: Electrophysiological evidence for loss of synaptic contacts in hippocampal field CA1 , 1992, Hippocampus.

[20]  J. O’Keefe,et al.  Phase relationship between hippocampal place units and the EEG theta rhythm , 1993, Hippocampus.

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

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

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

[24]  C. Barnes.  Normal aging: regionally specific changes in hippocampal synaptic transmission , 1994, Trends in Neurosciences.

[25]  J. Bolhuis,et al.  Retrograde Amnesia and Memory Reactivation in Rats with Ibotenate Lesions to the Hippocampus or Subiculum , 1994, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[26]  Bruce L. McNaughton,et al.  A Model of the Neural Basis of the Rat's Sense of Direction , 1994, NIPS.

[27]  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.

[28]  P Alvarez,et al.  Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  W E Skaggs,et al.  Deciphering the hippocampal polyglot: the hippocampus as a path integration system. , 1996, The Journal of experimental biology.

[30]  B. McNaughton,et al.  Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model , 1998, Hippocampus.

[31]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[33]  M. Gallagher,et al.  Neurobiological substrates of behavioral decline: Models and data analytic strategies for individual differences in aging , 1996, Neurobiology of Aging.

[34]  J. Lisman,et al.  Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. , 1996, Learning & memory.

[35]  C. Barnes,et al.  Age-related decrease in cholinergic synaptic transmission in three hippocampal subfields , 1996, Neurobiology of Aging.

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

[37]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  W E Skaggs,et al.  The Effect of Aging on Experience-Dependent Plasticity of Hippocampal Place Cells , 1997, The Journal of Neuroscience.

[39]  B. McNaughton,et al.  Multistability of cognitive maps in the hippocampus of old rats , 1997, Nature.

[40]  L. Nadel,et al.  Memory consolidation, retrograde amnesia and the hippocampal complex , 1997, Current Opinion in Neurobiology.

[41]  B L McNaughton,et al.  Path Integration and Cognitive Mapping in a Continuous Attractor Neural Network Model , 1997, The Journal of Neuroscience.

[42]  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.

[43]  M. Gallagher,et al.  The use of animal models to study the effects of aging on cognition. , 1997, Annual review of psychology.

[44]  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.

[45]  Building trust: health care leaders speak out--discussion. , 1998, Quality connection.

[46]  L. Nadel,et al.  Hippocampal contributions to cortical plasticity , 1998, Neuropharmacology.

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

[48]  Is drinking water sold in vending machines safe for people with HIV? , 1998, Positive living.

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

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

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

[52]  W. Mendelson,et al.  Age-related changes in sleep in the rat. , 1999, Sleep.

[53]  James L. McClelland,et al.  Neural models of memory , 1999, Current Opinion in Neurobiology.

[54]  M. Quirk,et al.  Interaction between spike waveform classification and temporal sequence detection , 1999, Journal of Neuroscience Methods.

[55]  M. Quirk,et al.  Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields , 2000, Neuron.

[56]  C. Barnes,et al.  Age-Related Decrease in the Schaffer Collateral-Evoked EPSP in Awake, Freely, Behaving Rats , 2000, Neural plasticity.

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

[58]  Arne D. Ekstrom,et al.  Dynamics of Hippocampal Ensemble Activity Realignment: Time versus Space , 2000, The Journal of Neuroscience.

[59]  Arne D. Ekstrom,et al.  NMDA Receptor Antagonism Blocks Experience-Dependent Expansion of Hippocampal “Place Fields” , 2001, Neuron.

[60]  B L McNaughton,et al.  Reactivation of hippocampal ensemble activity patterns in the aging rat. , 2001, Behavioral neuroscience.

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

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

[63]  Yutaka Kirino,et al.  Time-limited role of the hippocampus in the memory for trace eyeblink conditioning in mice , 2002, Brain Research.

[64]  Yutaka Kirino,et al.  Time-Dependent Reorganization of the Brain Components Underlying Memory Retention in Trace Eyeblink Conditioning , 2003, The Journal of Neuroscience.

[65]  B. McNaughton,et al.  Hippocampal map realignment and spatial learning , 2003, Nature Neuroscience.

[66]  Mark R. Bower,et al.  Off-line reprocessing of recent memory and its role in memory consolidation: a progress report , 2003 .

[67]  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.

[68]  M. Gallagher,et al.  Reduction in Size of Perforated Postsynaptic Densities in Hippocampal Axospinous Synapses and Age-Related Spatial Learning Impairments , 2004, The Journal of Neuroscience.

[69]  B. McNaughton,et al.  The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats , 1983, Experimental Brain Research.

[70]  Inah Lee,et al.  A Double Dissociation between Hippocampal Subfields Differential Time Course of CA3 and CA1 Place Cells for Processing Changed Environments , 2004, Neuron.

[71]  M. Gallagher,et al.  Aging, spatial learning, and total synapse number in the rat CA1 stratum radiatum , 2004, Neurobiology of Aging.

[72]  Eric A. Zilli,et al.  Gradual Translocation of Spatial Correlates of Neuronal Firing in the Hippocampus toward Prospective Reward Locations , 2006, Neuron.

[73]  C. Barnes,et al.  Neural plasticity in the ageing brain , 2006, Nature Reviews Neuroscience.

[74]  Bruce L McNaughton,et al.  Methodological Considerations on the Use of Template Matching to Study Long-Lasting Memory Trace Replay , 2006, The Journal of Neuroscience.

[75]  Inah Lee,et al.  The relationship between the field-shifting phenomenon and representational coherence of place cells in CA1 and CA3 in a cue-altered environment. , 2007, Learning & memory.

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

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

[78]  C. Barnes,et al.  Glutamate receptor-mediated restoration of experience-dependent place field expansion plasticity in aged rats. , 2008, Behavioral neuroscience.