Putting Fear in Its Place: Remapping of Hippocampal Place Cells during Fear Conditioning — TEI-tagged view

Moita, Rosis, Zhou, LeDoux, Blair · 2004 · neuroscience · doi:10.1523/jneurosci.5492-03.2004 · 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 rather than mechanism: the paper demonstrates that an aversive manipulation induces remapping and localises the cause to learned fear ('Furthermore, contextual fear conditioning caused significantly more remapping of place cells than auditory fear conditioning, suggesting that place cell remapping was related to the rat's learned fear of the environment.'), but it does not identify the physiological mechanism producing remapping; the functional account in the Discussion is offered as speculation ('It is tempting to speculate...'). The replicates relation covers the behavioural (freezing) result rather than the place-cell result. 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.
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
place cells13 remap partial remapping place field2 place maps correlation index peak shift spatial information3 spatial uniformity index fear conditioning3 contextual fear conditioning2 freezing5 conditioned stimulus2 unconditioned stimulus2 training box control box within-session stability-plasticity problem motivational valence movement of the recording electrode CA116 complex spike cells 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
phenomenonhippocampal place cell remapping during fear conditioning— “We recorded hippocampal place cells in two spatial environments: a training environment in which rats underwent fear conditioning and a neutral control environment.”
claim-typeexistence— “This finding indicates that aversive reinforcement can induce place cell remapping even when the environment itself remains unchanged.”
method — evidence— “Rats that were chronically implanted with hippocampal recording electrodes were placed in an experimental chamber in which they foraged for small food pellets dropped from an overhead dispenser ( Muller et al., 1987 ).”
object of study — evidence— “However, the causes and functional purpose of such remapping are poorly understood. In the present study, we addressed this question by investigating whether aversive conditioning induces place cell remapping.”
research question — evidence— “Furthermore, contextual fear conditioning caused significantly more remapping of place cells than auditory fear conditioning, suggesting that place cell remapping was related to the rat's learned fear of the environment. These results suggest that one possible function of place cell remapping may be to generate new spatial…
contribution — evidence— “We recorded hippocampal place cells in two spatial environments: a training environment in which rats underwent fear conditioning and a neutral control environment. Fear conditioning caused many place cells to alter (or remap) their preferred firing locations in the training environment, whereas most cells remained stable in the control…
transferfrom associative learning theory: the paired versus unpaired contingency design, which holds the stimuli constant and varies only what they predict— “place cell remapping was more pronounced in rats that primarily learned to fear the training environment (context group) compared with rats that primarily learned to fear the auditory CS (cued group), even though the stimuli (CS, US, and training box) in both tasks were the same”transfers[0]
transferfrom adaptive systems theory: the stability-plasticity dilemma, imported as the problem the hippocampus must be solving— “If it is true that place cell remapping allows the hippocampus to represent different states of a single environment, then the hippocampus must solve an intriguing stability-plasticity problem ( Grossberg, 1988 ), namely, place cells must somehow decide when the state of a given environment is stable versus when it has changed sufficiently to…transfers[1]
transferfrom image analysis: pixelwise correlation between two rate maps as the measure of whether a representation changed— “To further quantify the remapping of place cells caused by fear acquisition, we calculated two correlation indices for each place cell—one for the training ( r T ) and one for the control box ( r C )—by computing the pixel-by-pixel correlation between preconditioning and postconditioning place maps (see Materials and Methods). Low r values…transfers[2]
mechanismA change in the motivational valence of the environment triggers re-representation: the hippocampus rewrites its map so that the previously learned appetitive associations no longer attach to it, letting new aversive associations form on a fresh representation— “One possibility would be to alter the hippocampal representation of the environment itself, so that the previously learned appetitive associations would no longer be in force.”mechanisms[0]
mechanismRecoding the environment reduces competition between appetitive and aversive motivational drives that would arise if one representation carried both valences— “This may help to reduce competition between different motivational drives that might otherwise occur if a single environmental representation were permitted to acquire both appetitive and aversive motivational valence.”mechanisms[1]
mechanismRemapping is driven by predictive relevance rather than sensory input: cells remap when the environment itself is the best predictor of the reinforcer, because more remapped cells are then needed to carry the new contextual association— “This suggests that place cells are most likely to remap an environment in which aversive reinforcement occurs when the environment itself is the best predictor of reinforcement, which provides circumstantial evidence for the hypothesis that cells that remap are more involved in acquiring the new contextual association than non-remapping…mechanisms[2]
mechanisman environment that predicted food now predicts shock, and re-representing it lets aversive associations form without competing with the appetitive ones— “One possibility would be to alter the hippocampal representation of the environment itself, so that the previously learned appetitive associations would no longer be in force. Aversive associations could then quickly be formed with the new hippocampal representation, without competition from previously acquired appetitive associations.”mechanisms[3]
mechanismremapping poses a stability-plasticity problem: the cells must decide when an environment has changed enough to deserve a new representation— “If it is true that place cell remapping allows the hippocampus to represent different states of a single environment, then the hippocampus must solve an intriguing stability-plasticity problem ( Grossberg, 1988 ), namely, place cells must somehow decide when the state of a given environment is stable versus when it has changed sufficiently to…mechanisms[4]
mechanismpartial remapping may be the compromise - some cells carry the new associations while others preserve what was already learned— “It is possible that such partial remapping allows the hippocampus to compromise in its attempt to solve the stability-plasticity problem. That is, cells that remap their preferred firing location may allow rapid acquisition of new associations with the context, whereas cells that retain stable firing fields may help to preserve previously…mechanisms[5]
mechanismwhat drives remapping is what the animal learned, not the sensory events it received: both groups got the same tone, shock and box— “These results suggest that place cell remapping in the hippocampus is not strictly determined by the sensory characteristics of the…mechanisms[6]
extends Moita et al. (2003)claim_relations[0]
replicates Rescorla (1968); Phillips and LeDoux (1994)
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claim_relations[1]
builds-on Sharp (1999); Eichenbaum (2000)
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claim_relations[2]
extends the literature showing place fields are stable across repeated visits to one environment
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claim_relations[3]
extends prior reports of remapping when reinforcement location changes
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claim_relations[4]
qualifies the view that the hippocampal code represents the geometry of space
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claim_relations[5]
builds-on Moita et al. 2003, from the same recordings in the same rats
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claim_relations[6]
supports accounts in which the hippocampus encodes behavioural and temporal context within one environment
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claim_relations[7]
senseremapping here = a change of firing location across sessions in an UNCHANGED environment, not the classic sense of a change between two different environments
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senses[0]
sensepartial remapping = some cells remap and others do not IN THE SAME ANIMAL, so an average over cells describes no cell
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senses[1]
senseplace cell here is a filtered category: 53 of 154 recorded cells that passed three criteria are renamed place cells for the rest of the paper
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senses[2]
sensestable is defined numerically as r > 0.33 between pre and post maps, and is an INCLUSION criterion, not a result
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senses[3]
sensefreezing is operationalised as zero tracked movement for at least a third of a second, machine-scored, validated against human observers
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senses[4]
controlplace maps built ONLY from periods when the rat was moving — held — rules out freezing as a direct influence on the place maps - the fear-conditioned group froze far more (92 s against 57 s), and a stationary animal contributes no position samples, so freezing would otherwise shape the map itself
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controls[0]
controlthe post-conditioning session EXTENDED to 12 minutes for the context group against 10 for the cued group — held — rules out the number of position samples as the difference between groups - more freezing means fewer samples in a fixed session, and a sparser map remaps more readily for purely statistical reasons
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controls[1]
noteremap —operationalised-as→ correlation index — CRITERION: low r means the cell remapped, high r means the map held - the whole finding rests on this one number
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concept_edges[0]
noteremap —operationalised-as→ peak shift — a second, independent operationalisation of the same construct, reported alongside the first
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concept_edges[1]
weightremap —operationalised-as→ peak shift — 0.9
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concept_edges[1]
noteplace field —operationalised-as→ spatial information — one of three joint criteria: peak rate above 1.5 Hz, information above 0.2 bits/spike, at least 50 spikes
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concept_edges[2]
weightplace field —operationalised-as→ spatial information — 0.9
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concept_edges[2]
auditfreezing —operationalised-as→ fear conditioning — Audit 2026-09-28: DOUBTFUL - read against its span and kept, but freezing is the measured fear response; operationalised-as 'fear conditioning' names the procedure, not the construct.
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concept_edges[3]
notefreezing —operationalised-as→ fear conditioning — direction is measure-to-construct: freezing is the read-out of the learning, machine-scored
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concept_edges[3]
weightfreezing —operationalised-as→ fear conditioning — 0.9
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concept_edges[3]
notepartial remapping —is-a→ remap — a heterogeneous case of it: the population does not act as one, so a mean over cells describes no cell
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concept_edges[4]
notecontrol box —contrasted-with→ training box — the same cells in both, so the control environment is a within-cell baseline rather than a separate group
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concept_edges[6]
auditcontextual fear conditioning —is-a→ fear conditioning — Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span describes fear conditioning with cued and context groups; 'contextual fear conditioning' is not named, so is-a is loose.
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concept_edges[7]
auditEVIDENCE CORRECTED (RE-GROUNDED) · fear conditioning —causes→ remap — Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span writes 'conditioning' and 'remapped', not 'fear conditioning'.
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concept_edges[8]
evidential statusEVIDENCE CORRECTED (RE-GROUNDED) · fear conditioning —causes→ remap — the paper's own words: suggesting that
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concept_edges[8]
retractedEVIDENCE CORRECTED (RE-GROUNDED) · fear conditioning —causes→ remap — RE-GROUNDED. The old span is the STATISTICS of the effect, not the statement of it - '…s training = 13.95 +/- 1.78…' against the control box, with its t test - which names one endpoint and carries NO EFFECT CUE, so a 'causes' edge on it would fail the gate's causes test today. The replacement is the authors' own sentence for the same result: 'FEAR CONDITIONING CAUSED many…' place cells to remap in the training environment while most stayed stable in the control one. Both endpoints named, the verb is 'caused', and the control comparison is inside the span. THE NUMBERS ARE NOT LOST - they remain on the record as content tags and in the retracted span itself, which is why retraction-in-place matters.
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concept_edges[8]
weightplace cells —is-a→ complex spike cells — 0.9
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concept_edges[11]
auditspatial uniformity index —part-of→ place maps — Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the spatial uniformity index is COMPUTED OVER pixel bins of the place maps; part-of is loose.
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concept_edges[12]
notespatial uniformity index —part-of→ place maps — a control measure on the sampling behind the map, not on the map itself
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concept_edges[12]
weightspatial uniformity index —part-of→ place maps — 0.6
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concept_edges[12]
relationfear conditioning —causes→ remap — Fear conditioning caused many place cells to alter (or remap) their preferred firing locations
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concept_edges[13]
outcome (stated by the tagger, no quotation)control — heldcontrols[0]
outcome (stated by the tagger, no quotation)control — heldcontrols[1]
for which uselimitation — the persistence of the remapping: BECAUSE OF THE DIFFICULTIES ASSOCIATED WITH RECORDING THE SAME PLACE CELLS OVER MULTIPLE DAYS, WE WERE UNABLE TO ADDRESS THIS QUESTION
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limitations[0]
for which uselimitation — every behavioural-confound exclusion in the paper: IT IS NOT POSSIBLE TO CONTROL FOR EVERY POSSIBLE BEHAVIORAL INFLUENCE ON PLACE CELL ACTIVITY - the control set is partial by admission
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limitations[1]
for which uselimitation — the within-session stability control specifically: it excluded cells that gained or lost a field, so it does not cover the full population it is used to reassure about
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limitations[2]
for which uselimitation — the same scope as limitations[1] - not every behavioural influence can be controlled, and the controls are presented as several rather than exhaustive
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limitations[3]
for which uselimitation — the durability of the remapping: the one comparable effect WAS TEMPORARY, AND PLACE CELLS EVENTUALLY RESUMED THEIR ORIGINAL FIRING FIELDS, so whether this one lasts is unknown
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limitations[4]
for which uselimitation — the paper's central speculation, labelled as one: IT IS TEMPTING TO SPECULATE THAT PLACE CELLS THAT REMAP THEIR FIRING LOCATION IN RESPONSE TO A NOVEL REINFORCER ... ARE MORE LIKELY TO BECOME ASSOCIATED WITH THAT REINFORCER
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limitations[5]
for which uselimitation — the period immediately after conditioning, when the effect should be largest and cannot be measured: BECAUSE RATS WERE FREEZING ABOUT ONE-THIRD OF THE TIME ... IT WAS NOT POSSIBLE TO ANALYZE PLACE CELL ACTIVITY BECAUSE OF POOR SAMPLING OF THE ENVIRONMENT
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limitations[6]
for which uselimitation — the sample behind every remapping figure: 154 hippocampal cells were recorded and OF THESE, 53 COMPLEX SPIKE CELLS met criteria
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limitations[7]
for which uselimitation — the same scope as limitations[1] - IT IS NOT POSSIBLE TO CONTROL FOR EVERY POSSIBLE BEHAVIORAL INFLUENCE ON PLACE CELL ACTIVITY
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limitations[8]
replicationuntested
limitationThe study could not determine whether the conditioning-induced remapping is long-lasting or only temporary, because the same cells could not be followed across days.
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limitations[0]
limitationBehavioural confounds can only be partially ruled out; the authors control for several but concede the list cannot be exhaustive.
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limitations[1]
limitationThe within-session stability control excluded cells that gained or lost a field, so it does not cover the full remapping population.
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limitations[2]
limitationthe authors state outright that not every behavioural influence can be controlled, and present the controls as several rather than all
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limitations[3]
limitationwhether the remapping lasts is unknown, and the one comparable study found the effect temporary
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limitations[4]
limitationthe paper's own central speculation - that remapping cells are the ones that acquire the association - is declared hard to test
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limitations[5]
limitationat the moment the effect is strongest the measurement is impossible: freezing destroys the spatial sampling a place map needs
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limitations[6]
limitation53 of 154 recorded cells met inclusion criteria, and four of sixteen rats contributed none
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limitations[7]
limitationthe authors state that the controls are several, not exhaustive - 'It is not possible to control for every possible behavioral influence'
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limitations[8]
Content tags
content-observations: finding · quantity · variable · definition · key-term — grounded in the full text
findingFear conditioning made many CA1 place cells alter (remap) their preferred firing locations in the training box, while most cells stayed stable in the control box.
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content_tags.findings[0]
findingPixel-by-pixel correlations between pre- and post-conditioning maps were higher in the control box (0.59) than in the training box (0.39), confirming that remapping was specific to the conditioned environment.
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content_tags.findings[1]
findingThe peak of the place field moved about 14 cm in the training box versus about 9 cm in the control box after conditioning.
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content_tags.findings[2]
findingRemapping of the training box was more pronounced in rats trained with the context as the shock predictor (Z = -1.36) than with the tone (Z = -0.34).
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content_tags.findings[3]
findingConditioning changed only where cells fired, not how they fired: peak in-field rate, mean rate, spatial information content and field size were all unchanged in the training box.
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content_tags.findings[4]
findingWithin-session map stability in the training box was the same before (r = 0.57) and after (r = 0.56) conditioning.
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content_tags.findings[5]
findingRemapping was partial rather than global: within the same rat some cells kept their original firing fields while others moved theirs.
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content_tags.findings[6]
findingAfter conditioning, cued rats froze more to the tone while context rats froze more to the training context.
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content_tags.findings[7]
findingTheta-band power of the multiunit signal during place-cell spiking was not significantly changed by conditioning.
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content_tags.findings[8]
findingplace fields shifted further in the training box than in the control box
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content_tags.findings[9]
findingmap correlation was lower in the training box than the control box, 0.39 against 0.59
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content_tags.findings[10]
findingcontext-conditioned rats remapped the training box more than cue-conditioned rats
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content_tags.findings[11]
findingfiring rate, spatial information and field size were unchanged - only the location of firing moved
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content_tags.findings[12]
findingcells did not simply become unstable: within-session correlation was unchanged by conditioning
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content_tags.findings[13]
findingremapping is partial - within one animal some cells moved and others did not
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content_tags.findings[14]
findingcued rats froze more to the tone and context rats more to the box, confirming what each group had learned
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content_tags.findings[15]
findingno group difference in preferred circling direction after conditioning - one rat in the cued group and none in the context group switched
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content_tags.findings[16]
findingCONTROL NULL: freezing cannot have entered the place maps, because they include only periods when the rats were moving
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content_tags.findings[17]
findingCONTROL NULL: the two groups did not differ in where they spent time in the training box before versus after conditioning
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content_tags.findings[18]
findingCONTROL NULL: the two groups did not differ in how uniformly they foraged over the box while moving
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content_tags.findings[19]
findingCONTROL NULL: theta power during place cell spiking was not significantly changed by conditioning
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content_tags.findings[20]
quantity154 — total hippocampal theta and complex spike cells recorded across the 16 rats
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content_tags.quantities[0]
quantity53 — cells that met the inclusion criteria and were analysed as place cells, split 27 cued / 26 context
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content_tags.quantities[1]
quantityr C = 0.59 ± 0.04 and r T = 0.39 ± 0.05 — mean pre-to-post map correlation in the control box versus the training box
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content_tags.quantities[2]
quantity13.95 ± 1.78 / 8.76 ± 0.95 — mean shift in centimetres of the place-field peak in the training box versus the control box
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content_tags.quantities[3]
quantityZ context = -1.36 ± 0.33 and Z cued = -0.34 ± 0.25 — normalized training-box correlation score for the context group versus the cued group (more negative = more remapping)
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content_tags.quantities[4]
quantity>90% — agreement between the automated freezing measure and experienced human scorers
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content_tags.quantities[5]
quantity0.39 vs 0.59 — map correlation in the training box against the control box
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content_tags.quantities[6]
quantity13.95 vs 8.76 cm — peak field shift in the training box against the control box
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content_tags.quantities[7]
quantityr > 0.33 — the numerical definition of a stable field, used as an inclusion criterion against electrode drift
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content_tags.quantities[8]
quantity53 of 154 — recorded cells that met the inclusion criteria and are called place cells thereafter
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content_tags.quantities[9]
quantity18 cm/sec — speed floor for including position samples, so that freezing cannot enter the map
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content_tags.quantities[10]
quantity1.5 Hz, 0.2 bits/spike, 50 spikes — the three joint criteria for counting a place field in a session
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content_tags.quantities[11]
quantitymore than 90% — agreement between machine-scored freezing and experienced human observers
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content_tags.quantities[12]
quantity12 min vs 10 min — session length extended for the context group so sample counts matched despite more freezing
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content_tags.quantities[13]
variablecorrelation indices (dependent)
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content_tags.variables[1]
variablefreezing behavior (dependent)
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content_tags.variables[2]
variablenumber of position samples (control)
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content_tags.variables[4]
variablecorrelation index
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content_tags.variables[5]
variablepeak shift
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content_tags.variables[6]
variabletraining box
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content_tags.variables[7]
variablefreezing
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content_tags.variables[8]
definitionplace cells
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content_tags.definitions[0]
definitionremapping
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content_tags.definitions[1]
definitionpartial remapping
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content_tags.definitions[2]
definitionepisode of freezing
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content_tags.definitions[3]
definitionplace cells
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content_tags.definitions[5]
definitionremap
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content_tags.definitions[6]
definitionpartial remapping
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content_tags.definitions[7]
definitionfreezing
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content_tags.definitions[8]
definitionplace field
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content_tags.definitions[9]
definitionspatial uniformity index
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content_tags.definitions[10]
definitionstability-plasticity problem
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content_tags.definitions[11]
key-termsplace cells, remap, partial remapping, place field, place maps, CA1, fear conditioning, freezing, correlation index, motivational valence, stability-plasticity problem, spatial information
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.
ANOVA F as written: two-way ANOVA
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content_tags.statistics[0]
post hoc test p as written: Post hoc Newman-Keuls t tests
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content_tags.statistics[1]
paired t-test t as written: paired t (41) = 3.15; p = 0.003
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content_tags.statistics[2]
unpaired t-test t as written: unpaired t (14) = 1.22; p = 0.24
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content_tags.statistics[3]
correlation r as written: Pearson product-moment correlation ( r )
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content_tags.statistics[4]
z-score standardization Z as written: we computed a Z -score for each cell from both groups
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content_tags.statistics[5]
paired t test
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content_tags.statistics[6]
unpaired t
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content_tags.statistics[7]
two-way ANOVA
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content_tags.statistics[8]
Newman-Keuls
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content_tags.statistics[9]
Pearson product-moment correlation
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content_tags.statistics[10]
Z -score
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content_tags.statistics[11]
Second readings
a facet read a second time, independently, from its own sentence — and whether the two readings agree
claim typeexistence — a second reading reaching the same value; recorded: existence
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alternatives.claim_type
methodchronic tetrode recording of CA1 place cells in two boxes, before and after paired or unpaired tone-shock conditioning, with pixelwise map correlation — a second reading DIFFERING from the recorded value; recorded: electrophysiology
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alternatives.method
phenomenonplace cell remapping - a change of preferred firing location within an unchanged environment — a second reading DIFFERING from the recorded value; recorded: hippocampal place cell remapping during fear conditioning
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alternatives.phenomenon

When we have changed our mind. Some entries in the table begin with a word in capitals and the reason for it. EVIDENCE CORRECTED — the finding still stands, but we had quoted the wrong sentence from the paper, and the quotation has been replaced with the right one. RETRACTED — the entry itself was wrong; it stays on the page, marked, with the reason, rather than being deleted. WITHDRAWN AND REPLACED — the entry was wrong, and a corrected version of it appears in the entries below. Each mark carries its own reason, in brackets, because the reasons differ from one entry to the next. An entry we have WITHDRAWN is removed from this page and kept in the record, with its reason. A line reading Audit and a date is a later re-reading of the entry against its whole sentence: DOUBTFUL means it was kept, and the reason says what is loose about it. Quotation marks inside the tagger's sentence. Where a tag is the tagger's own sentence, a phrase in quotation marks inside it is borrowed from the paper — the tagger's wording around it is not. The paper's own sentence is the evidence quote for that row; on this page it is withheld with the article, and the article is at its publisher. Nothing inside quotation marks anywhere on this page is ours: if it is quoted, it is the paper's. Whose words a concept carries. A concept entry records a term the paper itself uses, so the term, the sense given for it, and its evidence are the paper's own words, quoted where the paper fixes them. This is the opposite of a sense entry in the tag table, which is the tagger's sentence about how the paper uses a term. Where a concept entry could not be grounded in the paper's words, the entry says so on its own row.

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