A neural substrate in the human hippocampus for linking successive events — TEI-tagged view

Paz, Gelbard-Sagiv, Mukamel, Harel, Malach, Fried · 2010 · neuroscience · doi:10.1073/pnas.0910834107 · full text at the source · TEI xml · tagged edition · index · concepts · authors
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.
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, whether or not the words occur in the text below — a number is how many papers in the corpus carry that tag; a tag with no number is unique to this paper
temporal relationships mutual information10 conditional entropy marginal entropy hippocampus29 entorhinal cortex7 amygdala10 anterior cingulate2 free recall6 free-viewing cell assemblies4 context-independent pure-stimulus electrophysiology110

Our tag layer for this paper

Cross-disciplinary analysis
content-tags & facets: phenomenon · claim-type · cross-domain-transfer · mechanism · claim-relation · replication-status · limitation — grounded in the full text
phenomenonmemory for the temporal order of events— “Memory formation includes knowledge about temporally dated events and the temporal relations of these events to each other.”
claim-typeexistence— “We found that neuronal activity in successive time segments became gradually correlated, and, as a result, activity in a given time window became a faithful predictor of the activity to follow.”
method — evidence— “Here we used recordings from single cells in the human brain obtained while subjects viewed repeated presentations of cinematic episodes.”
object of study — evidence— “However, it remains unclear how single cells and networks of cells can signal this temporal relationship between events.”
research question — evidence— “However, it remains unclear how single cells and networks of cells can signal this temporal relationship between events.”
contribution — evidence— “Importantly, this neuronal measure of temporal binding successfully predicted subjects’ ability to recall and verbally report the viewed episodes later.”
transferfrom information theory: mutual information and its decomposition into marginal and conditional entropy, used both as the measure and as the control on it— “Finally, we received further confirmation that our results stem from a developing relationship between successive time segments rather than from changes in the statistics of the firing rates by separately calculating the two components of the MI: the marginal entropy and the conditional entropy ( 31 ) Marginal entropy tests for changes in the…transfers[0]
transferfrom rodent hippocampal physiology: the paradigms requiring memory for temporal order, against which this free-viewing design is explicitly contrasted— “Moreover, most animal studies use paradigms in which learning takes many trials, and the animals typically are overtrained, but human memory can form following a single experience ( 1 – 4 ). Here, the neuronal changes already were seen during the second viewing, namely after only one viewing, as happens in real life episodic memory…transfers[1]
mechanismBecause 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— “the hippocampus is unique in its ability to integrate and take into account the successive events and the context in which they appeared ( 3 , 4 ), and thus it is capable of creating such branching representations.”mechanisms[0]
mechanismMemory 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— “The formation of memory here means that the representation of an external stimulus (a network state) would now converge internally and lead more reliably to the representation of other external stimuli (other network states) that followed in time.”mechanisms[1]
mechanismmutual information between successive time bins measures how much knowing activity now reduces uncertainty about activity next, which linear correlation cannot capture— “However, the relationship between subsequent activities does not have to be linear (i.e., low activity entails low activity and high entails high activity), and we therefore used a more appropriate measure: the mutual information (MI) ( 31 , 32 ) between subsequent time bins. This measure allowed us to unveil more complex relationships and…mechanisms[2]
mechanismthe analysis deliberately avoids assuming a constant representation, looking at a neuron's relation to itself over time rather than to the stimulus— “Another important aspect of our analysis is that it does not assume a constancy of the representation in a single neuron (i.e., linking a reproducible firing pattern to a repeated external event). Rather, it explores the relationship of a neuron to itself in consecutive times, thus taking into account the global state of the neural network at…mechanisms[3]
mechanismthe increase comes from reduced conditional entropy rather than raised marginal entropy, so it is the relationship changing and not the firing statistics— “Finally, we received further confirmation that our results stem from a developing relationship between successive time segments rather than from changes in the statistics of the firing rates by separately calculating the two components of the MI: the marginal entropy and the conditional entropy ( 31 ) Marginal entropy tests for changes in the…mechanisms[4]
mechanismthe hippocampus is proposed to be the site because it alone can integrate successive events with the context in which they occurred, allowing branching representations— “This neuronal correlate was detected in the hippocampus but not in other areas, probably due to the distinctive properties of the hippocampus: The temporal relationships we observed were context (clip)-specific. In real life, an event/stimulus can lead to many possible events/stimuli in different contexts and so can the specific neuronal…mechanisms[5]
mechanismmemories are framed as stable network states, with formation meaning one state leads more reliably to the next— “To conclude, our results support the conjecture that the brain encodes temporal information as changes in the state of the network ( 39 ) and that memories are encoded as stable states of neural networks ( 40 ). In this interpretation, the changes we see in the activity are changes in the internal representation of the external stimuli. The…mechanisms[6]
builds-on Hebb's original proposal (ref. 33) that neuronal assemblies can be linked temporally— “This finding is in line with Hebb's original proposal ( 33 ) that neuronal assemblies can be linked temporally and subserve the evolution of internal states in general ( 34 ) and episodic memory in particular ( 28 ).”claim_relations[0]
extends the same group's report of hippocampal reactivation during free recall, from the same experiments - a paper independently tagged in this corpusclaim_relations[1]
supports Hebb's proposal that neuronal assemblies can be linked temporallyclaim_relations[2]
supports fMRI evidence that hippocampal activation tracks retrieval of temporal order in naturalistic scenes
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
claim_relations[3]
qualifies the interpretation that the effect is growing visual familiarity
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claim_relations[4]
sensetemporal 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]
sensetwo 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]
sensethe 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]
sensememory 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]
controlthe clips re-shuffled so that the six viewings came from ENTIRELY DIFFERENT movie clips while staying within the same repetition number — held
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— rules out 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
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controls[0]
evidential statusfMRI evidence that hippocampal activation tracks retrieval of temporal order in naturalistic scenes — the paper's own words: we cannot rule out
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claim_relations[3]
audittemporal relationships —operationalised-as→ mutual information — Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span writes 'the relationship between subsequent activities', not 'temporal relationships'.
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concept_edges[0]
audittemporal relationships —causes→ free recall — 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.
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concept_edges[1]
notetemporal relationships —causes→ free recall — the paper says related directly to rather than causes; r = 0.87 across subjects. the weight carries the correlational status
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concept_edges[1]
weighttemporal relationships —causes→ free recall — 0.7
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concept_edges[1]
audithippocampus —distinct-from→ amygdala — 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.
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concept_edges[2]
notehippocampus —distinct-from→ amygdala — regional specificity is itself the control: an effect present only in hippocampus cannot be general arousal
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concept_edges[2]
notetemporal relationships —distinct-from→ context-independent — estimated separately in blank periods and subtracted, rather than assumed absent
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concept_edges[3]
weighttemporal relationships —distinct-from→ context-independent — 0.95
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concept_edges[3]
audittemporal relationships —distinct-from→ pure-stimulus — Audit 2026-09-28: DOUBTFUL - read against its span and kept, but the span describes stimulus correlations to be controlled; distinct-from is loose.
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concept_edges[4]
notetemporal relationships —distinct-from→ pure-stimulus — estimated by shuffling across repetitions of the same clip
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concept_edges[4]
weighttemporal relationships —distinct-from→ pure-stimulus — 0.95
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concept_edges[4]
outcomecontrol — held
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controls[0]
for which uselimitation — the learning interpretation: WE CANNOT RULE OUT THESE POSSIBLE CONTRIBUTIONS COMPLETELY - growing visual familiarity and improving retrieval both remain available
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limitations[0]
for which uselimitation — the assembly analysis: NEURAL ASSEMBLIES OF n > 3 REQUIRE MUCH LARGER AMOUNTS OF DATA AND COULD NOT BE MEASURED IN THE CURRENT PARADIGM
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limitations[1]
duplicate oflimitation — limitations[0]
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limitations[2]
for which uselimitation — the same scope as limitations[0] - the two alternative accounts are argued against, not excluded
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limitations[2]
for which uselimitation — 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
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limitations[3]
for which uselimitation — 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
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limitations[4]
for which uselimitation — any count of independent studies: THE SAME EXPERIMENTS WERE USED RECENTLY TO SHOW REACTIVATION OF NEURONAL ACTIVITY DURING FREE RECALL
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limitations[5]
for which uselimitation — the population and the recording sites: SINGLE AND MULTIUNITS WERE RECORDED (27 SESSIONS IN 13 INDIVIDUALS) in epilepsy patients whose implants follow clinical need
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limitations[6]
replicationuntested
limitationAlternative accounts in terms of growing visual familiarity or improved retrieval cannot be ruled out completely.
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limitations[0]
limitationAssemblies larger than three neurons could not be analysed with the data the paradigm yielded.
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limitations[1]
limitationtwo alternative interpretations - growing familiarity and improving retrieval - cannot be completely ruled out, and the authors say so
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limitations[2]
limitationthe familiarity account is argued against by an external finding rather than by a control in this dataset
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limitations[3]
limitationthe retrieval account would also fit the recall correlation, which the authors acknowledge
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limitations[4]
limitationthe data come from the same experiments already reported for a different finding
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limitations[5]
limitationsubjects are epilepsy patients implanted on purely clinical criteria
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limitations[6]
Content tags
content-observations: finding · quantity · variable · definition · key-term — grounded in the full text
findingWith 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]
findingThis 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]
findingThe 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]
findingThe 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]
findingThe 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]
findingDecomposing 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]
findingWhen 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]
findingJust 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]
findingactivity in successive time windows became mutually predictive across clip repetitions
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content_tags.findings[8]
findingthe effect emerged within two to three presentations
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content_tags.findings[9]
findingthe gradual increase appeared in hippocampus and not in amygdala, entorhinal cortex or anterior cingulate
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content_tags.findings[10]
findingonly in hippocampus did the effect exceed both rival sources of correlation
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content_tags.findings[11]
findingthe 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]
findingthe same result held with ordinary Pearson correlation instead of mutual information
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content_tags.findings[13]
findingthe rise in mutual information came from falling conditional entropy, not from changing firing statistics
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content_tags.findings[14]
findingoverall firing rate was stable across repetitions and along clip duration
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content_tags.findings[15]
findingno evidence of developing slow oscillations that could mimic the effect
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content_tags.findings[16]
quantityr = 0.87, P < 0.01 — across-subject correlation between hippocampal temporal relationships and free-recall success
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content_tags.quantities[0]
quantity54% (362/671) — proportion of all recorded neurons showing significant temporal relationships for at least one clip
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content_tags.quantities[1]
quantity52% (349/671) — proportion of recorded units classified as single units rather than multiunits
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content_tags.quantities[2]
quantityAH, 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]
quantityAH, 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]
quantity22% — proportion of neurons whose during-clip temporal relationships exceeded their context-independent (blank-period) relationships
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content_tags.quantities[5]
quantity250 ms — width of the time window into which spikes were binned for the main analysis
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content_tags.quantities[6]
quantityn = 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]
quantity671 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]
quantityr = 0.87, P < 0.01 — correlation between the hippocampal measure and individual recall
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content_tags.quantities[9]
quantity10 to 16 clips of 5 to 10 s, each repeated six times — the viewing design
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content_tags.quantities[10]
quantitywithin two to three presentations — how fast the effect emerged
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content_tags.quantities[11]
variablebrain structure (moderator)
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content_tags.variables[1]
variablemutual information (dependent)
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content_tags.variables[2]
variablememory performance (dependent)
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content_tags.variables[3]
variablenumber of spikes (control)
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content_tags.variables[4]
definitiontemporal relationships
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content_tags.definitions[0]
definitionpure-stimulus relationships
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content_tags.definitions[1]
definitioncontext-independent correlations
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content_tags.definitions[2]
definitionresponsive neurons
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content_tags.definitions[3]
definitiontemporal relationships
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content_tags.definitions[4]
key-termstemporal relationships, mutual information, conditional entropy, marginal entropy, hippocampus, entorhinal cortex, amygdala, anterior cingulate, free recall, free-viewing, cell assemblies, episodic memory, temporal binding, single units, epilepsy, clip, repetition, Hebb, shuffling, linear regression
Statistics — cross-field join keys
field-invariant statistical terms, used in their statistical sense (gated on a number / symbol / test). A p-value or a standard deviation means the SAME thing in physics, biology, psychology and sociology — so these are the strongest cross-field join keys. Grounded verbatim.
mutual information MI as written: mutual information (MI)
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[0]
correlation as written: Pearson correlation coefficient
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[1]
regression as written: linear regression
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[2]
t-test as written: t tests
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[3]
multiple-comparison correction as written: Bonferron-corrected
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[4]
chi-squared χ 2 as written: χ 2
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[5]
ANOVA as written: two-way ANOVA
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[6]
Fisher's exact test
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[7]
Fisher's combined probability test as written: Fisher's combined test
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[8]
permutation (shuffle) test as written: we shuffled the time windows within each clip
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[9]
Mann-Whitney U test as written: Mann–Whitney nonparametric test
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[10]
bias correction of an estimator as written: analytical bias correction
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[11]
mutual information between successive time windows
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[12]
shuffling across repetitions
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[13]
Fisher's combined test
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[14]
marginal and conditional entropy decomposition
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
content_tags.statistics[15]
Second readings
a facet read a second time, independently, from its own sentence — and whether the two readings agree
methodsingle-unit recording in epilepsy patients freely viewing repeated audiovisual clips, with mutual information between successive time windows as the measure — a second reading DIFFERING from the recorded value; recorded: electrophysiology
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
alternatives.method
phenomenontemporal binding during episodic memory formation — a second reading DIFFERING from the recorded value; recorded: memory for the temporal order of events
Quotation withheld — this paper is not ours to reproduce, and the page has already quoted as much of it as the rights layer allows. The tag, its field and its confidence stand; the sentence is at the publisher.
alternatives.phenomenon

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