A neural substrate in the human hippocampus for linking successive events

Paz, Gelbard-Sagiv, Mukamel, Harel, Malach, Fried · Proceedings of the National Academy of Sciences · 2010 · neuroscience · 10.1073/pnas.0910834107 · record Paz2010-a-neural-substrate-in-the-human-hippocampus
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Where this record's text came from. faceted 2026-08 by reading the locally held text (html); every evidence string verified as an exact substring of that text before merging. Claim type is 'existence' because the paper's shape is the demonstration that a hippocampus-specific neuronal correlate of temporal binding exists and tracks behaviour; the discussion offers a mechanistic interpretation (memories as network states) but does not test it. Only one claim_relation is recorded: the article cites almost entirely by bare reference number, and rule 7 forbids inferring relations from bare citations, so the sentences relating the work to refs 29, 10 and 35 were left out; Hebb is named in running text, so that one qualifies. No statement in the paper reports anyone testing or repeating these findings, hence replication status untested. 2026-08-13 and 2026-08-15 schema-0.3 passes: every quote verified as an exact substring of the staged text and anchored at merge time; concept terms verified present; every edge endpoint an existing node.
7 quotations on this page contain a reference number where the paper printed a superscript. This journal style prints citations as raised numerals — parameters12,13 — and the extraction flattened them into the line, so the sentence reads parameters 12 , 13 . The digits are citation markers and not part of what the author wrote. The quotes keep them for the same reason they keep every other extraction fault: a quote is reproduced exactly or it proves nothing.
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Other fields define these differently the same word, defined another way in another discipline
episodic memory 3 fields · linear regression 2 fields · Pearson correlation coefficient 2 fields

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 13 concept tags on this paper, none is 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.
temporal relationships mutual information conditional entropy marginal entropy hippocampus entorhinal cortex amygdala anterior cingulate free recall free-viewing cell assemblies context-independent pure-stimulus Because the hippocampus alone integrates successive events together with the context in which they occurred, it can build context-specific branching representations, which is why the developing temporal linkage appears there and not in amygdala or cingulate cortex Memory formation is the internal convergence of one network state onto the network state representing the stimulus that followed it in time, so that each state comes to lead reliably to the next episodic memory temporal binding single units epilepsy clip repetition Hebb shuffling linear regression pure-stimulus relationships context-independent correlations responsive neurons brain structure memory performance number of spikes mutual information (MI) correlation Pearson correlation coefficient regression t-test t tests multiple-comparison correction Bonferron-corrected chi-squared ANOVA two-way ANOVA Fisher's exact test Fisher's combined probability test Fisher's combined test permutation (shuffle) test we shuffled the time windows within each clip Mann-Whitney U test Mann–Whitney nonparametric test bias correction of an estimator analytical bias correction mutual information between successive time windows shuffling across repetitions marginal and conditional entropy decomposition electrophysiology

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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
concept edgeconcept_edgesan asserted relation between two concepts, with the sentence asserting 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
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transfertransfersa method or concept carried in from another field

The paper

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Every tag on this page

alternatives 2 · claim_relations 5 · claim_type 1 · concept_edges 5 · content_tags 54 · contribution 1 · controls 1 · limitations 7 · mechanisms 7 · method 1 · object_of_study 1 · phenomenon 1 · research_question 1 · senses 4 · transfers 2

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facettagfieldconf.whose words
object_of_studyhow single human neurons come to signal the temporal relationship between successive events
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object_of_studythe paper's words
research_questionhow neuronal activity patterns evolve as memory for the temporal order of events is formed
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research_questionthe paper's words
contributionshows hippocampal activity in successive time segments becomes mutually predictive across repetitions, specifically in hippocampus, and that this predicts each subject's later free recall
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contributionthe paper's words
claim_typeexistence
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claim_typethe paper's words
phenomenonmemory for the temporal order of events
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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
mechanismsmutual information between successive time bins measures how much knowing activity now reduces uncertainty about activity next, which linear correlation cannot capture
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mechanisms[2]1.0the tagger's words
mechanismsthe analysis deliberately avoids assuming a constant representation, looking at a neuron's relation to itself over time rather than to the stimulus
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mechanisms[3]1.0the tagger's words
mechanismsthe increase comes from reduced conditional entropy rather than raised marginal entropy, so it is the relationship changing and not the firing statistics
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mechanisms[4]1.0the tagger's words
mechanismsthe hippocampus is proposed to be the site because it alone can integrate successive events with the context in which they occurred, allowing branching representations
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mechanisms[5]0.9the tagger's words
mechanismsmemories are framed as stable network states, with formation meaning one state leads more reliably to the next
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mechanisms[6]0.95the tagger's words
limitationsAlternative accounts in terms of growing visual familiarity or improved retrieval cannot be ruled out completely.
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what this limits: the learning interpretation: WE CANNOT RULE OUT THESE POSSIBLE CONTRIBUTIONS COMPLETELY - growing visual familiarity and improving retrieval both remain available
limitations[0]the tagger's words
limitationsAssemblies larger than three neurons could not be analysed with the data the paradigm yielded.
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what this limits: the assembly analysis: NEURAL ASSEMBLIES OF n > 3 REQUIRE MUCH LARGER AMOUNTS OF DATA AND COULD NOT BE MEASURED IN THE CURRENT PARADIGM
limitations[1]the tagger's words
limitationstwo alternative interpretations - growing familiarity and improving retrieval - cannot be completely ruled out, and the authors say so
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duplicate of: limitations[0] · what this limits: the same scope as limitations[0] - the two alternative accounts are argued against, not excluded
limitations[2]1.0the tagger's words
limitationsthe familiarity account is argued against by an external finding rather than by a control in this dataset
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what this limits: the familiarity rebuttal specifically, whose evidence is external: IT WAS SHOWN RECENTLY THAT THE TOTAL NUMBER OF SPIKES ELICITED IN A HIPPOCAMPAL [response does not grow with familiarity] - a result from another paper, not a control here
limitations[3]1.0the tagger's words
limitationsthe retrieval account would also fit the recall correlation, which the authors acknowledge
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what this limits: the correlation with subsequent memory: THIS INTERPRETATION ALSO WOULD FIT WITH THE REMARKABLE CORRELATION WE FOUND BETWEEN THE NEURONAL MEASURE AND THE SUBSEQUENT INDIVIDUAL MEMORY, so the headline result does not discriminate between the accounts
limitations[4]1.0the tagger's words
limitationsthe data come from the same experiments already reported for a different finding
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what this limits: any count of independent studies: Quotation withheld
limitations[5]1.0the tagger's words
limitationssubjects are epilepsy patients implanted on purely clinical criteria
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what this limits: the population and the recording sites: SINGLE AND MULTIUNITS WERE RECORDED (27 SESSIONS IN 13 INDIVIDUALS) in epilepsy patients whose implants follow clinical need
limitations[6]0.8the tagger's words
transfersmutual information and its decomposition into marginal and conditional entropy, used both as the measure and as the control on it
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transfers[0]1.0the tagger's words
transfersthe paradigms requiring memory for temporal order, against which this free-viewing design is explicitly contrasted
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transfers[1]1.0the tagger's words
controlsthe clips re-shuffled so that the six viewings came from ENTIRELY DIFFERENT movie clips while staying within the same repetition number
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eliminates: the experimental context - the room - and the mere passage of time as the source of the temporal relationships, both of which advance identically whichever clip is shown · outcome: held
controls[0]0.95the tagger's words
sensestemporal relationships is defined operationally as mutual information between spike counts in successive time windows, expressed as a percentage of the maximum possible information
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senses[0]1.0the tagger's words
sensestwo rival sources of the same correlation are named and separately estimated: context-independent drift, measured in blank periods, and pure-stimulus structure, measured by shuffling across repetitions
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senses[1]1.0the tagger's words
sensesthe free-viewing paradigm is defended as closer to real memory formation than animal paradigms, because it uses no reinforcement and needs no overtraining
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senses[2]1.0the tagger's words
sensesmemory formation is recast as a change in which network state reliably follows which, rather than as a change in what a neuron represents
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senses[3]1.0the tagger's words
alternativesmethod: single-unit recording in epilepsy patients freely viewing repeated audiovisual clips, with mutual information between successive time windows as the measure
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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: temporal binding during episodic memory formation
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a second reading DIFFERING from the recorded value. Recorded: memory for the temporal order of events — 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 → Hebb's original proposal (ref. 33) that neuronal assemblies can be linked temporally
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claim_relations[0]the tagger's words
claim_relationsextends → the same group's report of hippocampal reactivation during free recall, from the same experiments - a paper independently tagged in this corpus
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claim_relations[1]1.0the tagger's words
claim_relationssupports → Hebb's proposal that neuronal assemblies can be linked temporally
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claim_relations[2]1.0the tagger's words
claim_relationssupports → fMRI evidence that hippocampal activation tracks retrieval of temporal order in naturalistic scenes
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status: the paper's own words: we cannot rule out
claim_relations[3]0.85the tagger's words
claim_relationsqualifies → the interpretation that the effect is growing visual familiarity
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claim_relations[4]1.0the tagger's words
concept_edgestemporal relationships —operationalised-as→ mutual information
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strength of the relation: 1 Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span writes 'the relationship between subsequent activities', not 'temporal relationships'.
concept_edges[0]1.0the tagger's words
concept_edgestemporal relationships —causes→ free recall
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strength of the relation: 0.7 · note: the paper says related directly to rather than causes; r = 0.87 across subjects. the weight carries the correlational status Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but temporal relationships are 'RELATED DIRECTLY TO' memory performance across subjects; causes overstates an association.
concept_edges[1]1.0the tagger's words
concept_edgeshippocampus —distinct-from→ amygdala
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strength of the relation: 1 · note: regional specificity is itself the control: an effect present only in hippocampus cannot be general arousal Audit 2026-09-28: DOUBTFUL - read against its span and kept, but the span reports a gradual increase in the hippocampus but not other structures; distinct-from is loose.
also in: hippocampus · amygdala
concept_edges[2]1.0the tagger's words
concept_edgestemporal relationships —distinct-from→ context-independent
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strength of the relation: 0.95 · note: estimated separately in blank periods and subtracted, rather than assumed absent
concept_edges[3]1.0the tagger's words
concept_edgestemporal relationships —distinct-from→ pure-stimulus
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strength of the relation: 0.95 · note: estimated by shuffling across repetitions of the same clip Audit 2026-09-28: DOUBTFUL - read against its span and kept, but the span describes stimulus correlations to be controlled; distinct-from is loose.
concept_edges[4]1.0the tagger's words
content_tagsmutual information
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content_tags.statistics[0]the tagger's words
content_tagscorrelation
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also in: correlation
content_tags.statistics[1]the tagger's words
content_tagsregression
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also in: regression
content_tags.statistics[2]the tagger's words
content_tagst-test
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also in: t-test
content_tags.statistics[3]the tagger's words
content_tagsmultiple-comparison correction
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content_tags.statistics[4]the tagger's words
content_tagschi-squared
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also in: chi-squared
content_tags.statistics[5]the tagger's words
content_tagsANOVA
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also in: ANOVA
content_tags.statistics[6]the tagger's words
content_tagsFisher's exact test
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content_tags.statistics[7]the tagger's words
content_tagsFisher's combined probability test
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content_tags.statistics[8]the tagger's words
content_tagspermutation (shuffle) test
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content_tags.statistics[9]the tagger's words
content_tagsMann-Whitney U test
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content_tags.statistics[10]the tagger's words
content_tagsbias correction of an estimator
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content_tags.statistics[11]the tagger's words
content_tagsmutual information between successive time windows
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content_tags.statistics[12]1.0the tagger's words
content_tagsshuffling across repetitions
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content_tags.statistics[13]1.0the tagger's words
content_tagsFisher's combined test
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content_tags.statistics[14]0.9the tagger's words
content_tagsmarginal and conditional entropy decomposition
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content_tags.statistics[15]1.0the tagger's words
content_tagsWith repeated viewing, activity in successive time segments became gradually correlated, so activity in one window came to predict the activity that followed.
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content_tags.findings[0]the tagger's words
content_tagsThis linkage appeared after only two or three viewings of an episode and was stronger than both context-independent and stimulus-driven correlations.
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content_tags.findings[1]the tagger's words
content_tagsThe gradual growth of temporal relationships across clip repetitions occurred in the hippocampus only, not in amygdala, anterior cingulate or entorhinal cortex at the single-cell level.
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content_tags.findings[2]the tagger's words
content_tagsThe strength of hippocampal temporal relationships during viewing predicted how many clips a subject later recalled freely, with a correlation of 0.87 across subjects.
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content_tags.findings[3]the tagger's words
content_tagsThe effect was not an artifact of changing firing rates, because mean firing rate was stable across both clip repetition and clip duration.
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content_tags.findings[4]the tagger's words
content_tagsDecomposing mutual information showed the rise came from falling conditional entropy (better prediction of the next window) rather than from rising marginal entropy (changed firing statistics).
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content_tags.findings[5]the tagger's words
content_tagsWhen simultaneously recorded pairs and triplets of cells were analysed, a significant increase in temporal relationships appeared in entorhinal cortex as well.
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content_tags.findings[6]the tagger's words
content_tagsJust over half of all recorded neurons (362 of 671) showed a significant increase in temporal relationships for at least one clip.
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content_tags.findings[7]the tagger's words
content_tagsactivity in successive time windows became mutually predictive across clip repetitions
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content_tags.findings[8]1.0the tagger's words
content_tagsthe effect emerged within two to three presentations
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content_tags.findings[9]1.0the tagger's words
content_tagsthe gradual increase appeared in hippocampus and not in amygdala, entorhinal cortex or anterior cingulate
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content_tags.findings[10]1.0the tagger's words
content_tagsonly in hippocampus did the effect exceed both rival sources of correlation
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content_tags.findings[11]1.0the tagger's words
content_tagsthe measure correlated with each subject's later free recall at r = 0.87, and in no other structure
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content_tags.findings[12]1.0the tagger's words
content_tagsthe same result held with ordinary Pearson correlation instead of mutual information
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content_tags.findings[13]1.0the tagger's words
content_tagsthe rise in mutual information came from falling conditional entropy, not from changing firing statistics
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content_tags.findings[14]1.0the tagger's words
content_tagsoverall firing rate was stable across repetitions and along clip duration
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content_tags.findings[15]1.0the tagger's words
content_tagsno evidence of developing slow oscillations that could mimic the effect
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content_tags.findings[16]1.0the tagger's words
content_tagstemporal relationships
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content_tags.definitions[0]the tagger's words
content_tagspure-stimulus relationships
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content_tags.definitions[1]the tagger's words
content_tagscontext-independent correlations
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content_tags.definitions[2]the tagger's words
content_tagsresponsive neurons
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content_tags.definitions[3]the tagger's words
content_tagstemporal relationships
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content_tags.definitions[4]1.0the tagger's words
content_tagsbrain structure
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content_tags.variables[1]the tagger's words
content_tagsmutual information
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content_tags.variables[2]the tagger's words
content_tagsmemory performance
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content_tags.variables[3]the tagger's words
content_tagsnumber of spikes
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content_tags.variables[4]the tagger's words
content_tagsr = 0.87, P < 0.01 — across-subject correlation between hippocampal temporal relationships and free-recall success
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content_tags.quantities[0]the tagger's words
content_tags54% (362/671) — proportion of all recorded neurons showing significant temporal relationships for at least one clip
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content_tags.quantities[1]the tagger's words
content_tags52% (349/671) — proportion of recorded units classified as single units rather than multiunits
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content_tags.quantities[2]the tagger's words
content_tagsAH, n = 180; amygdala n = 160; EC n = 224; AC n = 107 — number of units recorded in each brain structure across 27 sessions in 13 patients
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content_tags.quantities[3]the tagger's words
content_tagsAH, 49%; EC, 34%; amygdala, 23%; AC, 25% — proportion of neurons per structure whose temporal relationships exceeded the pure-stimulus baseline
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content_tags.quantities[4]the tagger's words
content_tags22% — proportion of neurons whose during-clip temporal relationships exceeded their context-independent (blank-period) relationships
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content_tags.quantities[5]the tagger's words
content_tags250 ms — width of the time window into which spikes were binned for the main analysis
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content_tags.quantities[6]the tagger's words
content_tagsn = 4,884 pairs and n = 2,1061 triplets — number of simultaneously recorded cell pairs and triplets analysed for assembly-level temporal relationships
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content_tags.quantities[7]the tagger's words
content_tags671 units in 27 sessions from 13 individuals; hippocampus 180, amygdala 160, entorhinal 224, anterior cingulate 107 — the recorded sample
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content_tags.quantities[8]1.0the tagger's words
content_tagsr = 0.87, P < 0.01 — correlation between the hippocampal measure and individual recall
Quotation withheld — this record is not cleared for redistribution. The sentence is in the paper at the link above.
content_tags.quantities[9]1.0the tagger's words
content_tags10 to 16 clips of 5 to 10 s, each repeated six times — the viewing design
Quotation withheld — this record is not cleared for redistribution. The sentence is in the paper at the link above.
content_tags.quantities[10]1.0the tagger's words
content_tagswithin two to three presentations — how fast the effect emerged
Quotation withheld — this record is not cleared for redistribution. The sentence is in the paper at the link above.
content_tags.quantities[11]1.0the tagger's words

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