CoChat
Sign Up
Cited by 1,709Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

Two-stage model of memory trace formation: A role for “noisy” brain states

Buzsáki, G.·1989·Neuroscience
DOI 10.1016/0306-4522(89)90423-5
Open this paper in CoChat — free account

Abstract

Review of the normally occurring neuronal patterns of the hippocampus suggests that the two principal cell types of the hippocampus, the pyramidal neurons and granule cells, are maximally active during different behaviors. Granule cells reach their highest discharge rates during theta-concurrent exploratory activities, while population synchrony of pyramidal cells is maximum during immobility, consummatory behaviors, and slow wave sleep associated with field sharp waves. Sharp waves reflect the summed postsynaptic depolarization of large numbers of pyramidal cells in the CA1 and subiculum as a consequence of synchronous discharge of bursting CA3 pyramidal neurons. The trigger for the population burst in the CA3 region is the temporary release from subcortical tonic inhibition. An overview of the experimentally explored criteria of synaptic enhancement (intensity, frequency, and pattern of postsynaptic depolarization, calcium influx, cooperativity, threshold) suggests that these requirements may be present during sharp wave-concurrent population bursts of pyramidal cells. Experimental evidence is cited showing that (a) population bursts in CA3 may lead to long-term potentiation in their postsynaptic CA1 targets, (b) tetanizing stimuli are capable of increasing the synchrony of the sharp wave-burst, and (c) activity patterns of the neocortical input to the hippocampus determine which subgroup of CA3 neurons will trigger subsequently occurring population bursts (initiator cells). Based on the experimental evidence reviewed a formal model of memory trace formation is outlined. During exploratory (theta) behaviors the neocortical information is transmitted to the hippocampus via the fast-firing granule cells which may induce a weak and transient heterosynaptic potentiation in a subgroup of CA3 pyramidal cells. The weakly potentiated CA3 neurons will then initiate population bursts upon the termination of exploratory activity (sharp wave state). It is assumed that recurrent excitation during the population burst is strongest on those cells which initiated the population event. It is suggested that the strong excitatory drive brought about by the sharp wave-concurrent population bursts during consummatory behaviors, immobility, and slow wave sleep may be sufficient for the induction of long-term synaptic modification in the initiator neurons of the CA3 region and in their targets in CA1. In this two-stage model both exploratory (theta) and sharp wave states of the hippocampus are essential and any interference that might modify the structure of the population bursts (e.g. epileptic spikes) is detrimental to memory trace formation.

Integrity signals

Registry

Crossref · 10.1016/0306-4522(89)90423-5

Cites

156 of 156 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • During SWS, firing patterns observed during waking are replayed at a much faster (10-20 times) rate.

    “1) during SWS, firing patterns observed during waking are replayed at a much faster (10 -20 times) rate, suggesting a time-compressed form of memory reactivation (160, 551, 606, 715, 843, 1090);”

    From About Sleep's Role in Memory (2013) · cites this paper as [160]

  • In the hippocampus, memory stabilization is thought to be supported by sleep reactivation, whereby assembly firing patterns expressed during exploration are reactivated in subsequent sleep/rest periods during sharp wave/ripple oscillatory events.

    “In the hippocampus memory stabilization is thought to be supported by ‘sleep reactivation’ whereby assembly firing patterns expressed during exploration are reactivated in subsequent sleep/rest periods during sharp wave/ripple (SWR, 135–250Hz) oscillatory events11,12.”

    From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [11]

  • Such reactivation is thought to enable the incorporation of new memory engrams, especially those associated with novel and rewarded outcomes, into stable representations capable of informing future behavior.

    “Such reactivation is thought to enable the incorporation of new memory engrams, especially those associated with novel and rewarded outcomes, into stable representations capable of informing future behavior6,11,12,18.”

    From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [11]

Cites

Flagged first, then by citations

4 of the 160 references couldn’t be matched to a known paper.

Cited by

Sorted by citations

Related

Authors
Buzsáki, G.
Affiliations
University of California System (US)
Corresponding author
Buzsáki, G.
ORCID
Buzsáki, G.
Venue
Neuroscience
Publisher
Elsevier BV
Published
1989-01
Volume
31
Issue
3
Pages
551-570
ISSN
0306-4522 (ISSN-L)
DOI
10.1016/0306-4522(89)90423-5
OpenAlex
W2020272049
Cited by
1,709
References
160
Citations by year
2026: 43 · 2025: 63 · 2024: 74 · 2023: 86 · 2022: 64 · 2021: 67 · 2020: 65 · 2019: 86 · 2018: 73 · 2017: 70 · 2016: 56 · 2015: 64 · 2014: 80 · 2013: 66 · 2012: 53
FWCI
2.53
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
memory trace formation, hippocampus, sharp-wave ripples, CA3 pyramidal cells, CA1, granule cells, theta oscillations, population bursts, long-term potentiation, synaptic plasticity, slow-wave sleep, recurrent excitation, two-stage model
MeSH terms
Animals, Hippocampus, Memory, Models, Neurological, Neuronal Plasticity, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review