Putting Fear in Its Place: Remapping of Hippocampal Place Cells during Fear Conditioning

Putting Fear in Its Place: Remapping of Hippocampal Place Cells during Fear Conditioning Moita Rosis Zhou LeDoux Blair

Tag layer of the DHSS Meta-Tagging Project. The article text is reproduced from the staged copy named in sourceDesc and is not altered; the tags are held separately in standOff so that overlapping and nested spans are preserved.

Putting Fear in Its Place: Remapping of Hippocampal Place Cells during Fear Conditioning 2004 Journal of Neuroscience 10.1523/jneurosci.5492-03.2004 Moita2004-putting-fear-in-its-place-remapping-of-hippo Moita2004-putting-fear-in-its-place-remapping-of-hippo.txt, the project's staged copy a82db992b48225d483bf3436da376600a83502cd not-redistributable neuroscience

the paper's own words

the tag layer; a sentence written by the tagger about the paper, always anchored to a quotation but not itself a quotation

0 spans located by searching the stored text for the quote's exact words, allowing any whitespace between them whether learning to fear a place changes the hippocampal map of that place, with the place itself unchanged Quotation withheld because this record is not cleared for redistribution. whether aversive conditioning induces place cell remapping, and whether the amount of remapping tracks what the animal learned rather than what it was shown Quotation withheld because this record is not cleared for redistribution. shows fear conditioning remaps place cells in the training environment but not a control environment, and remaps more when the context rather than a tone predicts shock Quotation withheld because this record is not cleared for redistribution. existence Quotation withheld because this record is not cleared for redistribution. hippocampal place cell remapping during fear conditioning Quotation withheld because this record is not cleared for redistribution. electrophysiology electrophysiology Quotation withheld because this record is not cleared for redistribution. mechanisms A 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 Quotation withheld because this record is not cleared for redistribution. mechanisms Recoding the environment reduces competition between appetitive and aversive motivational drives that would arise if one representation carried both valences Quotation withheld because this record is not cleared for redistribution. mechanisms Remapping 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 Quotation withheld because this record is not cleared for redistribution. an environment that predicted food now predicts shock, and re-representing it lets aversive associations form without competing with the appetitive ones Quotation withheld because this record is not cleared for redistribution. remapping poses a stability-plasticity problem: the cells must decide when an environment has changed enough to deserve a new representation Quotation withheld because this record is not cleared for redistribution. partial remapping may be the compromise - some cells carry the new associations while others preserve what was already learned Quotation withheld because this record is not cleared for redistribution. what drives remapping is what the animal learned, not the sensory events it received: both groups got the same tone, shock and box Quotation withheld because this record is not cleared for redistribution. The 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. what this limits: 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 Quotation withheld because this record is not cleared for redistribution. Behavioural confounds can only be partially ruled out; the authors control for several but concede the list cannot be exhaustive. what this limits: 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 Quotation withheld because this record is not cleared for redistribution. The within-session stability control excluded cells that gained or lost a field, so it does not cover the full remapping population. what this limits: 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 Quotation withheld because this record is not cleared for redistribution. the authors state outright that not every behavioural influence can be controlled, and present the controls as several rather than all what this limits: the same scope as limitations[1] - not every behavioural influence can be controlled, and the controls are presented as several rather than exhaustive Quotation withheld because this record is not cleared for redistribution. whether the remapping lasts is unknown, and the one comparable study found the effect temporary what this limits: 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 Quotation withheld because this record is not cleared for redistribution. the paper's own central speculation - that remapping cells are the ones that acquire the association - is declared hard to test what this limits: 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 Quotation withheld because this record is not cleared for redistribution. at the moment the effect is strongest the measurement is impossible: freezing destroys the spatial sampling a place map needs what this limits: 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 Quotation withheld because this record is not cleared for redistribution. 53 of 154 recorded cells met inclusion criteria, and four of sixteen rats contributed none what this limits: the sample behind every remapping figure: 154 hippocampal cells were recorded and OF THESE, 53 COMPLEX SPIKE CELLS met criteria Quotation withheld because this record is not cleared for redistribution. the authors state that the controls are several, not exhaustive - 'It is not possible to control for every possible behavioral influence' what this limits: the same scope as limitations[1] - IT IS NOT POSSIBLE TO CONTROL FOR EVERY POSSIBLE BEHAVIORAL INFLUENCE ON PLACE CELL ACTIVITY Quotation withheld because this record is not cleared for redistribution. the paired versus unpaired contingency design, which holds the stimuli constant and varies only what they predict Quotation withheld because this record is not cleared for redistribution. the stability-plasticity dilemma, imported as the problem the hippocampus must be solving Quotation withheld because this record is not cleared for redistribution. pixelwise correlation between two rate maps as the measure of whether a representation changed Quotation withheld because this record is not cleared for redistribution. place maps built ONLY from periods when the rat was moving eliminates: 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 · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. the post-conditioning session EXTENDED to 12 minutes for the context group against 10 for the cued group eliminates: 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 · outcome (stated by the tagger, no quotation): held Quotation withheld because this record is not cleared for redistribution. remapping here = a change of firing location across sessions in an UNCHANGED environment, not the classic sense of a change between two different environments Quotation withheld because this record is not cleared for redistribution. partial remapping = some cells remap and others do not IN THE SAME ANIMAL, so an average over cells describes no cell Quotation withheld because this record is not cleared for redistribution. place 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 Quotation withheld because this record is not cleared for redistribution. stable is defined numerically as r > 0.33 between pre and post maps, and is an INCLUSION criterion, not a result Quotation withheld because this record is not cleared for redistribution. freezing is operationalised as zero tracked movement for at least a third of a second, machine-scored, validated against human observers Quotation withheld because this record is not cleared for redistribution. claim_type: existence 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. Quotation withheld because this record is not cleared for redistribution. method: chronic 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 — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. phenomenon: place 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 — note: a second reading, verbatim-verified, disagreeing with the value on the record. Not applied - a person decides. Quotation withheld because this record is not cleared for redistribution. extends → Moita et al. (2003) Quotation withheld because this record is not cleared for redistribution. replicates → Rescorla (1968); Phillips and LeDoux (1994) Quotation withheld because this record is not cleared for redistribution. builds-on → Sharp (1999); Eichenbaum (2000) Quotation withheld because this record is not cleared for redistribution. extends → the literature showing place fields are stable across repeated visits to one environment Quotation withheld because this record is not cleared for redistribution. extends → prior reports of remapping when reinforcement location changes Quotation withheld because this record is not cleared for redistribution. qualifies → the view that the hippocampal code represents the geometry of space Quotation withheld because this record is not cleared for redistribution. builds-on → Moita et al. 2003, from the same recordings in the same rats Quotation withheld because this record is not cleared for redistribution. supports → accounts in which the hippocampus encodes behavioural and temporal context within one environment Quotation withheld because this record is not cleared for redistribution. remap —operationalised-as→ correlation index remap correlation index strength of the relation: 1 · note: CRITERION: low r means the cell remapped, high r means the map held - the whole finding rests on this one number Quotation withheld because this record is not cleared for redistribution. remap —operationalised-as→ peak shift remap peak shift strength of the relation: 0.9 · note: a second, independent operationalisation of the same construct, reported alongside the first Quotation withheld because this record is not cleared for redistribution. place field —operationalised-as→ spatial information place field spatial information strength of the relation: 0.9 · note: one of three joint criteria: peak rate above 1.5 Hz, information above 0.2 bits/spike, at least 50 spikes Quotation withheld because this record is not cleared for redistribution. freezing —operationalised-as→ fear conditioning freezing fear conditioning strength of the relation: 0.9 · note: direction is measure-to-construct: freezing is the read-out of the learning, machine-scored 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. Quotation withheld because this record is not cleared for redistribution. partial remapping —is-a→ remap partial remapping remap strength of the relation: 1 · note: a heterogeneous case of it: the population does not act as one, so a mean over cells describes no cell Quotation withheld because this record is not cleared for redistribution. control box —contrasted-with→ training box control box training box strength of the relation: 1 · note: the same cells in both, so the control environment is a within-cell baseline rather than a separate group Quotation withheld because this record is not cleared for redistribution. contextual fear conditioning —is-a→ fear conditioning contextual fear conditioning fear conditioning strength of the relation: 1 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. Quotation withheld because this record is not cleared for redistribution. EVIDENCE CORRECTED (RE-GROUNDED) · fear conditioning —causes→ remap fear conditioning remap EVIDENCE CORRECTED: 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. — status: the paper's own words: suggesting that · strength of the relation: 1 Audit 2026-09-28: DOUBTFUL - read against its full span and kept, but the span writes 'conditioning' and 'remapped', not 'fear conditioning'. Quotation withheld because this record is not cleared for redistribution. place cells —is-a→ complex spike cells place cells complex spike cells strength of the relation: 0.9 Quotation withheld because this record is not cleared for redistribution. spatial uniformity index —part-of→ place maps spatial uniformity index place maps strength of the relation: 0.6 — the record marks this weak · note: a control measure on the sampling behind the map, not on the map itself 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. Quotation withheld because this record is not cleared for redistribution. fear conditioning —causes→ remap fear conditioning remap the relation itself is separately evidenced · strength of the relation: 1 · the relation stated: Fear conditioning caused many place cells to alter (or remap) their preferred firing locations Quotation withheld because this record is not cleared for redistribution. ANOVA ANOVA Quotation withheld because this record is not cleared for redistribution. post hoc test post hoc test Quotation withheld because this record is not cleared for redistribution. paired t-test paired t-test Quotation withheld because this record is not cleared for redistribution. unpaired t-test unpaired t-test Quotation withheld because this record is not cleared for redistribution. correlation correlation Quotation withheld because this record is not cleared for redistribution. z-score standardization z-score standardization Quotation withheld because this record is not cleared for redistribution. paired t test paired t test Quotation withheld because this record is not cleared for redistribution. unpaired t unpaired t Quotation withheld because this record is not cleared for redistribution. two-way ANOVA two-way ANOVA Quotation withheld because this record is not cleared for redistribution. Newman-Keuls Newman-Keuls Quotation withheld because this record is not cleared for redistribution. Pearson product-moment correlation Pearson product-moment correlation Quotation withheld because this record is not cleared for redistribution. Z -score Z -score Quotation withheld because this record is not cleared for redistribution. Fear 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. Quotation withheld because this record is not cleared for redistribution. Pixel-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. Quotation withheld because this record is not cleared for redistribution. The peak of the place field moved about 14 cm in the training box versus about 9 cm in the control box after conditioning. Quotation withheld because this record is not cleared for redistribution. Remapping 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). Quotation withheld because this record is not cleared for redistribution. Conditioning 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. Quotation withheld because this record is not cleared for redistribution. Within-session map stability in the training box was the same before (r = 0.57) and after (r = 0.56) conditioning. Quotation withheld because this record is not cleared for redistribution. Remapping was partial rather than global: within the same rat some cells kept their original firing fields while others moved theirs. Quotation withheld because this record is not cleared for redistribution. After conditioning, cued rats froze more to the tone while context rats froze more to the training context. Quotation withheld because this record is not cleared for redistribution. Theta-band power of the multiunit signal during place-cell spiking was not significantly changed by conditioning. Quotation withheld because this record is not cleared for redistribution. place fields shifted further in the training box than in the control box Quotation withheld because this record is not cleared for redistribution. map correlation was lower in the training box than the control box, 0.39 against 0.59 Quotation withheld because this record is not cleared for redistribution. context-conditioned rats remapped the training box more than cue-conditioned rats Quotation withheld because this record is not cleared for redistribution. firing rate, spatial information and field size were unchanged - only the location of firing moved Quotation withheld because this record is not cleared for redistribution. cells did not simply become unstable: within-session correlation was unchanged by conditioning Quotation withheld because this record is not cleared for redistribution. remapping is partial - within one animal some cells moved and others did not Quotation withheld because this record is not cleared for redistribution. cued rats froze more to the tone and context rats more to the box, confirming what each group had learned Quotation withheld because this record is not cleared for redistribution. no group difference in preferred circling direction after conditioning - one rat in the cued group and none in the context group switched Quotation withheld because this record is not cleared for redistribution. CONTROL NULL: freezing cannot have entered the place maps, because they include only periods when the rats were moving Quotation withheld because this record is not cleared for redistribution. CONTROL NULL: the two groups did not differ in where they spent time in the training box before versus after conditioning Quotation withheld because this record is not cleared for redistribution. CONTROL NULL: the two groups did not differ in how uniformly they foraged over the box while moving Quotation withheld because this record is not cleared for redistribution. CONTROL NULL: theta power during place cell spiking was not significantly changed by conditioning Quotation withheld because this record is not cleared for redistribution. place cells place cells Quotation withheld because this record is not cleared for redistribution. remapping remapping Quotation withheld because this record is not cleared for redistribution. partial remapping partial remapping Quotation withheld because this record is not cleared for redistribution. episode of freezing episode of freezing Quotation withheld because this record is not cleared for redistribution. place cells place cells Quotation withheld because this record is not cleared for redistribution. remap remap Quotation withheld because this record is not cleared for redistribution. partial remapping partial remapping Quotation withheld because this record is not cleared for redistribution. freezing freezing Quotation withheld because this record is not cleared for redistribution. place field place field Quotation withheld because this record is not cleared for redistribution. spatial uniformity index spatial uniformity index Quotation withheld because this record is not cleared for redistribution. stability-plasticity problem stability-plasticity problem Quotation withheld because this record is not cleared for redistribution. correlation indices correlation indices Quotation withheld because this record is not cleared for redistribution. freezing behavior freezing behavior Quotation withheld because this record is not cleared for redistribution. number of position samples number of position samples Quotation withheld because this record is not cleared for redistribution. correlation index correlation index Quotation withheld because this record is not cleared for redistribution. peak shift peak shift Quotation withheld because this record is not cleared for redistribution. training box training box Quotation withheld because this record is not cleared for redistribution. freezing freezing Quotation withheld because this record is not cleared for redistribution. 154 — total hippocampal theta and complex spike cells recorded across the 16 rats Quotation withheld because this record is not cleared for redistribution. 53 — cells that met the inclusion criteria and were analysed as place cells, split 27 cued / 26 context Quotation withheld because this record is not cleared for redistribution. r 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 Quotation withheld because this record is not cleared for redistribution. 13.95 ± 1.78 / 8.76 ± 0.95 — mean shift in centimetres of the place-field peak in the training box versus the control box Quotation withheld because this record is not cleared for redistribution. Z 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) Quotation withheld because this record is not cleared for redistribution. >90% — agreement between the automated freezing measure and experienced human scorers Quotation withheld because this record is not cleared for redistribution. 0.39 vs 0.59 — map correlation in the training box against the control box Quotation withheld because this record is not cleared for redistribution. 13.95 vs 8.76 cm — peak field shift in the training box against the control box Quotation withheld because this record is not cleared for redistribution. r > 0.33 — the numerical definition of a stable field, used as an inclusion criterion against electrode drift Quotation withheld because this record is not cleared for redistribution. 53 of 154 — recorded cells that met the inclusion criteria and are called place cells thereafter Quotation withheld because this record is not cleared for redistribution. 18 cm/sec — speed floor for including position samples, so that freezing cannot enter the map Quotation withheld because this record is not cleared for redistribution. 1.5 Hz, 0.2 bits/spike, 50 spikes — the three joint criteria for counting a place field in a session Quotation withheld because this record is not cleared for redistribution. more than 90% — agreement between machine-scored freezing and experienced human observers Quotation withheld because this record is not cleared for redistribution. 12 min vs 10 min — session length extended for the context group so sample counts matched despite more freezing Quotation withheld because this record is not cleared for redistribution.

The full text of this article is not redistributable, so it is not included here. The evidence sentences are withheld with it; the tag layer and its grounding status remain. The article itself is at https://doi.org/10.1523/jneurosci.5492-03.2004.