Reactivation of hippocampal ensemble memories during sleep

Wilson, McNaughton · Science · 1994 · neuroscience · 10.1126/science.8036517 · record Wilson1994-reactivation-of-hippocampal-ensemble-memorie
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Tags on this paper

Every tag the record carries, each linking to every other paper in the corpus that carries it. A tag appears here whether or not its words occur in the article — the spans below are only the ones a sentence in this paper licenses. Of the 5 concept tags on this paper, all 5 are grounded in a quoted sentence. All carry the tagger's gloss of what the term means in this paper, which is not something the article can license.
place fields cross-correlations ripples autoassociative memory synaptic modification Waking experience drives associative synaptic modification, which leaves cells that were coactive during behaviour more likely to be reactivated together in subsequent slow-wave sleep Event memory is first stored by rapid synaptic modification in the hippocampus, and is then replayed during slow-wave sleep (when further hippocampal modification is suppressed) so that the information is gradually transferred to neocortex Initial storage of the event occurs through rapid synaptic modification primarily within the hippocampus itself amount of overlap cross-correlation of spike trains significant spatial firing overlap ANOVA analysis of variance cross-correlation Spike-train cross-correlations mean Mean crosscorrelations correlation electrophysiology

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second readingalternativesan independent re-reading of a facet, recorded whether or not it agrees
relation to other workclaim_relationshow this paper stands to another: agrees, contradicts, extends, qualifies
claim typeclaim_typethe shape of the claim: existence, mechanism, method, critique, prediction, null
conceptconceptsan idea the paper works with, quoted where the paper uses it
content tagcontent_tagsa finding, definition, quantity, statistic or variable named in the paper
contributioncontributionwhat the paper claims to add
controlcontrolsan experiment run to eliminate a rival explanation
limitationlimitationswhat the paper says its evidence cannot support
mechanismmechanismshow the reported effect is said to come about
methodmethodhow the paper produced its evidence
object of studyobject_of_studywhat the paper is about — the thing it investigates
phenomenonphenomenonthe effect or regularity under study
research questionresearch_questionthe question the paper sets itself
sensesensesa distinct use of a term, quoted where the paper fixes it

The paper

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Every tag on this page

alternatives 3 · claim_relations 4 · claim_type 1 · concepts 5 · content_tags 30 · contribution 1 · controls 4 · limitations 5 · mechanisms 6 · method 1 · object_of_study 1 · phenomenon 1 · research_question 1 · senses 4

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facettagfieldconf.whose words
object_of_studythe activity correlations between pairs of hippocampal CA1 cells, measured across sleep before behaviour, behaviour, and sleep after it
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object_of_studythe paper's words
research_questionwhether the interactions among hippocampal cells change in a way SPECIFIC to the experience just had, rather than changing in general
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research_questionthe paper's words
contributionthe first demonstration that cells coactive during behaviour become more correlated in the sleep that follows, while cells that were active and NOT coactive do not
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contributionthe paper's words
claim_typeexistence
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claim_typethe paper's words
phenomenonhippocampal ensemble reactivation during sleep
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phenomenonthe paper's words
methodelectrophysiology
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methodthe paper's words
mechanismsmechanisms
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mechanisms[0]the tagger's words
mechanismsmechanisms
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mechanisms[1]the tagger's words
mechanismsmechanisms
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mechanisms[2]the tagger's words
mechanismsan autoassociative network in which RECURRENT EXCITATION reproduces a stored activity pattern from very little input - so background noise alone can push the network into a stored state, seen as a population burst
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mechanisms[3]0.95the tagger's words
mechanismsrandom background noise occasionally lands the network in a correlated state, and the resulting population bursts ARE the ripples - the paper's account of why the effect appears in discrete events rather than continuously
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mechanisms[4]0.95the tagger's words
mechanismsstorage is fast synaptic modification in the hippocampus during waking; sleep is the playback, and the transfer target is neocortex
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mechanisms[5]0.95the tagger's words
limitationsThe increased correlation implies associative synaptic change somewhere in the system, but not necessarily inside the hippocampus.
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limitations[0]the tagger's words
limitationsNeocortical or subcortical changes are an alternative source of the increased correlations.
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limitations[1]the tagger's words
limitationsTHE PAPER REFUSES TO LOCATE ITS OWN MECHANISM. The increased correlation is called consistent with associative synaptic modification `at some stage in the system, although not necessarily in the hippocampus` - the structure it recorded from
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limitations[2]0.95the tagger's words
limitationsa PAIR-WISE correlation cannot show that the activity is organised into a coherent representation; the paper says the prior single-cell result was suggestive and could not settle it, which is the same limit its own measure has
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limitations[3]0.95the tagger's words
limitationsthe population encoding any one event is expected to be small, so the whole design depends on recording enough cells for the pair count to grow as the square
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limitations[4]0.95the tagger's words
controlscell pairs that were ACTIVE during running but NOT COACTIVE - non-overlapping place fields - are measured through the same PRE and POST sleep sessions as the coactive pairs
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eliminates: any explanation that would raise correlations across the board: arousal, electrode drift, general post-behaviour excitability, or a recording artefact of the sleep session itself · outcome: held
controls[0]0.95the tagger's words
controlsthe RUN phase is checked first for the effect the sorting assumes - that overlapping place fields do produce correlated firing and non-overlapping ones do not
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eliminates: a sort that does not separate what it claims to, which would make the POST comparison meaningless in either direction · outcome: held
controls[1]0.95the tagger's words
controlsthe correlation is computed separately DURING ripples and in the intervals between them
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eliminates: an effect spread evenly through sleep, which would not support the proposed burst-based transfer mechanism · outcome: absent-not-in-staged-text
controls[2]0.85the tagger's words
controlswhether the correlation increase can be localised to the hippocampus at all
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eliminates: nothing - the paper states the modification may be at some other stage in the system · outcome: absent-declared-unreported
controls[3]0.95the tagger's words
conceptsplace fields
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also in: place fields
concepts[0]0.95the paper's words
conceptscross-correlations
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concepts[1]0.95the paper's words
conceptsripples
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also in: ripples
concepts[2]0.95the paper's words
conceptsautoassociative memory
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concepts[3]0.95the paper's words
conceptssynaptic modification
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concepts[4]0.95the paper's words
sensesreactivation - AS MEASURED HERE: an increase in the short-latency cross-correlation of a cell PAIR from PRE to POST sleep. Not a replayed sequence, not a retrieved memory, not a hippocampal event specifically - the instrument sees a pair statistic and the title names a memory. The paper marks that gap twice rather than closing it
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senses[0]0.95the tagger's words
sensesmemory, AS THE PAPER USES IT HERE: `the structure of distributed representations of the visited locations`, retained across sleep. The definition is spatial and population-level, and it is what the overlap-sorted pairs operationalise
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senses[1]0.95the tagger's words
sensesripple - a synchronised intermittent burst during slow-wave sleep, identified with the EEG sharp wave. Used here as the WINDOW in which the correlation effect is concentrated, and as the network signature of a stored pattern being re-entered
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senses[2]0.95the tagger's words
sensesthe ripple/inter-ripple split - the paper's own test of where in sleep the effect lives. The design is stated plainly; its RESULT is the one sentence in this record that OCR damage puts out of reach, and the control below says so rather than borrowing a verdict from its neighbour
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senses[3]0.85the tagger's words
alternativesclaim_type: existence
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a second reading reaching the same value. Recorded: existence — note: a second reading reaching the same value from a different sentence. Not applied - a person decides.
alternatives.claim_typethe tagger's words
alternativesmethod: simultaneous recording of 50 to 100 CA1 cells, short-latency spike-train cross-correlation computed per pair over each of three phases, pairs sorted by how much their place fields overlap
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a second reading DIFFERING from the recorded value. Recorded: electrophysiology — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides.
alternatives.methodthe tagger's words
alternativesphenomenon: experience-specific reactivation - coactivity acquired during waking behaviour re-expressed in hippocampal circuits during subsequent slow-wave sleep
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a second reading DIFFERING from the recorded value. Recorded: hippocampal ensemble reactivation during sleep — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides.
alternatives.phenomenonthe tagger's words
claim_relationsbuilds-on → previous theoretical models of autoassociative memory (ref. 6)
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claim_relations[0]the tagger's words
claim_relationsextends → the large-ensemble recording method itself, used here because the number of observable pair-wise interactions grows as the square of the cells recorded - the argument that makes an experience-specific effect measurable at all
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claim_relations[1]0.95the tagger's words
claim_relationscritiques → the indirect synaptic-efficacy evidence for hippocampal learning, on the ground that no change had been shown that was SPECIFIC to a given experience
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claim_relations[2]0.95the tagger's words
claim_relationssupports → autoassociative network models in which recurrent excitation reconstructs a stored pattern from little input
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claim_relations[3]0.95the tagger's words
content_tagsANOVA
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also in: ANOVA
content_tags.statistics[0]the tagger's words
content_tagscross-correlation
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content_tags.statistics[1]the tagger's words
content_tagsmean
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also in: mean
content_tags.statistics[2]the tagger's words
content_tagscross-correlations
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content_tags.statistics[3]0.95the tagger's words
content_tagscorrelation
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also in: correlation
content_tags.statistics[4]0.95the tagger's words
content_tagsHippocampal CA1 cells that fired together during a spatial behavioural task showed increased tendency to fire together in the sleep that followed, relative to the sleep that preceded the task.
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content_tags.findings[0]the tagger's words
content_tagsThe increase was specific to coactive pairs: cells silent during behaviour, and active cells whose place fields did not overlap, showed no such increase.
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content_tags.findings[1]the tagger's words
content_tagsCoactive (overlapping place field) pairs rose significantly above their pre-behaviour correlation level, whereas pairs of spatially firing cells with non-overlapping fields did not.
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content_tags.findings[2]the tagger's words
content_tagsThe reactivation effect decayed across the post-behaviour sleep session with a time constant of about 12 minutes.
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content_tags.findings[3]the tagger's words
content_tagsThe sleep correlations were concentrated in the synchronized population bursts (ripples) rather than in the intervals between them.
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content_tags.findings[4]the tagger's words
content_tagsDuring running, cells with overlapping place fields were strongly positively correlated while non-overlapping pairs were not, confirming the grouping used for the sleep comparison.
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content_tags.findings[5]the tagger's words
content_tagscells coactive during behaviour show a SIGNIFICANT INCREASE in correlation from PRE to POST sleep, and pairs that fired spatially but not in the same region do not - the effect is specific to shared experience, not to having been active
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content_tags.findings[6]0.95the tagger's words
content_tagsTHE PAPER DECLINES TO PLACE ITS OWN MECHANISM: the increase is consistent with associative synaptic modification at some stage in the system, ALTHOUGH NOT NECESSARILY IN THE HIPPOCAMPUS
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content_tags.findings[7]0.95the tagger's words
content_tagsthe sorting variable is validated before it is used - during RUN, overlapping place fields are highly positively correlated and non-overlapping ones are not
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content_tags.findings[8]0.95the tagger's words
content_tagslarge simultaneously recorded ensembles were studied because the number of observable pair interactions grows as the SQUARE of the sample size
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content_tags.findings[9]0.95the tagger's words
content_tagswaking activity retains the structure of distributed representations of the visited locations across sleep - stated as the paper's conclusion
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content_tags.findings[10]0.95the tagger's words
content_tagsintermittent, synchronized bursts in which cells discharge during slow-wave sleep, associated with EEG sharp-wave activity
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also in: ripples
content_tags.definitions[1]0.95the tagger's words
content_tagsa model in which recurrent excitation reproduces a previously stored activity pattern even when the input contains very little of the relevant information
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content_tags.definitions[2]0.95the tagger's words
content_tagsamount of overlap
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content_tags.variables[1]the tagger's words
content_tagscross-correlation of spike trains
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content_tags.variables[2]the tagger's words
content_tagssignificant spatial firing
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content_tags.variables[3]the tagger's words
content_tagsplace fields
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also in: place fields
content_tags.variables[4]0.95the tagger's words
content_tagsoverlap
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also in: overlap
content_tags.variables[5]0.95the tagger's words
content_tagsapproximately 12 min — time constant of the decay of the reactivated correlation during post-behaviour sleep
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content_tags.quantities[0]the tagger's words
content_tagsrat 1: 49 cells; rat 2: 74 cells; rat 3: 69 cells — number of simultaneously recorded hippocampal pyramidal cells in each of the three rats
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content_tags.quantities[1]the tagger's words
content_tags50 to 100 — number of single CA1 cells monitored simultaneously in each recording session
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content_tags.quantities[2]the tagger's words
content_tagsNON 437 and OVR 60; NON 719 and OVR 95; NON 941 and OVR 147 — numbers of non-overlapping versus overlapping cell pairs contributing to the histograms for rats 1, 2 and 3
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content_tags.quantities[3]the tagger's words
content_tagsP < 0.05 — significance level at which the post-run correlation increase for coactive pairs was established by ANOVA
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content_tags.quantities[4]the tagger's words
content_tagsapproximately 20 min — duration of each of the PRE, RUN and POST recording periods
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content_tags.quantities[5]the tagger's words
content_tagsminutes - the approximate duration of each of the three phases, PRE, RUN and POST
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content_tags.quantities[6]0.95the tagger's words

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