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W4385250143 abstract "Full text Figures and data Side by side Abstract Editor's evaluation eLife digest Introduction Results Discussion Methods Data availability References Decision letter Author response Article and author information Metrics Abstract Aversive stimuli can cause hippocampal place cells to remap their firing fields, but it is not known whether remapping plays a role in storing memories of aversive experiences. Here, we addressed this question by performing in vivo calcium imaging of CA1 place cells in freely behaving rats (n = 14). Rats were first trained to prefer a short path over a long path for obtaining food reward, then trained to avoid the short path by delivering a mild footshock. Remapping was assessed by comparing place cell population vector similarity before acquisition versus after extinction of avoidance. Some rats received shock after systemic injections of the amnestic drug scopolamine at a dose (1 mg/kg) that impaired avoidance learning but spared spatial tuning and shock-evoked responses of CA1 neurons. Place cells remapped significantly more following remembered than forgotten shocks (drug-free versus scopolamine conditions); shock-induced remapping did not cause place fields to migrate toward or away from the shocked location and was similarly prevalent in cells that were responsive versus non-responsive to shocks. When rats were exposed to a neutral barrier rather than aversive shock, place cells remapped significantly less in response to the barrier. We conclude that place cell remapping occurs in response to events that are remembered rather than merely perceived and forgotten, suggesting that reorganization of hippocampal population codes may play a role in storing memories for aversive events. Editor's evaluation This paper describes important results obtained from multi-cellular imaging of CA1 cells using large-field-of-view miniscopes in rats performing a shock avoidance task. By exploiting behavioral (barriers) and pharmacological (scopolamine) manipulations the authors provide convincing results on cell remapping dynamics during aversive learning. This work will be of interest for the neuroscience community by setting new methodological standards and providing data for across species comparisons. https://doi.org/10.7554/eLife.80661.sa0 Decision letter Reviews on Sciety eLife's review process eLife digest The human brain is able to remember experiences that occurred at specific places and times, such as a birthday party held at a particular restaurant. A part of the brain known as the hippocampus helps to store these episodic memories, but how exactly is not fully understood. Within the hippocampus are specialized neurons known as place cells which ‘label’ locations with unique patterns of brain activity. When we revisit a place, such as the restaurant, place cells recall the stored pattern of brain activity allowing us to recognize the familiar location. It has been shown that a new negative experience at a familiar place – for example, if we went back to the restaurant and had a terrible meal – triggers place cells to update the brain activity label associated with the location. However, it remains uncertain whether this re-labelling assists in storing the memory of the unpleasant experience. To investigate, Blair et al. used a technique known as calcium imaging to monitor place cells in the hippocampus of freely moving rats. The rats were given a new experience – a mild foot shock – at a previously explored location. Tiny cameras attached to their heads were then used to record the activity of hundreds of place cells before and after the shock. Initially, the rats remembered the aversive experience and avoided the location where they had been shocked. Over time, the rats began to return to the location; however, their place cells displayed different patterns of activity compared to their previous visits before the shock. To test whether this change in place cell activity corresponded with new memories, another group of rats were administered a mild amnesia-inducing drug before the shock, causing them to forget the experience. These rats did not avoid the shock site or show any changes in place cell activity when they revisited it. These findings imply that new events cause place cells to alter their ‘label’ for a location only if the event is remembered, not if it is forgotten. This indicates that alterations in place cell activity patterns may play a role in storing memories of unpleasant experiences. Having a better understanding of how episodic memories are stored could lead to better treatments for diseases that impair memory, such as Alzheimer’s disease and age-related dementia. Introduction The rodent hippocampus contains place cells that fire selectively during visits to specific locations in space (O’Keefe and Dostrovsky, 1971). When place cells were first discovered, they were hypothesized to encode ‘cognitive maps’ that store stable long-lasting memories for the spatial geometry of familiar environments (O’Keefe and Nadel, 1978). Supporting this view, electrophysiology studies showed that place cells can retain stable positional tuning across repeated visits to the same environment (Lever et al., 2002). However, methodological limitations of single-unit electrophysiology made it challenging to consistently record the same population of place cells across long time spans, and thus to investigate the duration of time over which place cell tuning properties remained stable. Recent advances in in vivo calcium imaging have made it possible to perform longitudinal studies of place cell tuning over days or weeks of experience. Such studies suggest that place cells in mice (Ziv et al., 2013; Cai et al., 2016; Kinsky et al., 2018; Keinath et al., 2022) and to a lesser extent in rats (Wirtshafter and Disterhoft, 2022) can change their spatial tuning properties (i.e., ‘remap’) with the mere passage time (see also Mankin et al., 2012). This phenomenon suggests that place cells may not simply encode spatial maps of environmental geometry, but also encode mnemonic information about accumulated past experiences that have occurred within an environment (Leutgeb et al., 2005; Colgin et al., 2008; Mankin et al., 2012; Ziv et al., 2013; Cai et al., 2016; Sanders et al., 2020). If so, then the rate at which place cells remap over time within a given environment may be proportional to the rate at which an animal stores new episodic memories of events that are linked to that environment. If the rate of place remapping reflects the rate of hippocampal memory storage, then motivationally significant events (such as encounters with appetitive or aversive stimuli) that are preferentially stored to episodic memory might be expected to accelerate the rate of place cell remapping within environments where such events occur. Consistent with this view, studies have shown that place cells remap in response to behaviorally significant events (Breese et al., 1989; Bostock et al., 1991; Hollup et al., 2001; Colgin et al., 2008; Dupret et al., 2010; Alvernhe et al., 2011; Mamad et al., 2017). Numerous studies have shown that when an aversive stimulus is encountered in an environment, place cells respond by remapping their firing fields in that environment (Moita et al., 2003; Moita et al., 2004; Wang et al., 2012; Wang et al., 2015; Kim et al., 2015; Mamad et al., 2019; Schuette et al., 2020; Ormond et al., 2023), but it is not well understood whether such remapping plays a role in storing memories of aversive experiences. Here, we investigated the role of place cell remapping in memory by using the MiniLFOV (Guo et al., 2023), a recently developed large-field-of-view version of the UCLA Miniscope (Cai et al., 2016; Aharoni and Hoogland, 2019), to image population activity of CA1 place cells in freely behaving rats as they acquired and extinguished a spatial avoidance learning task. The task was performed on a rectangular maze where rats ran stereotyped linear trajectories, allowing the speed and direction of running behavior to be closely matched during sessions conducted before acquisition versus after extinction of avoidance learning. In agreement with prior studies, we observed that avoidance learning induced place cell remapping in an environment where footshock was encountered compared with control conditions where (1) rats encountered a neutral barrier instead of an aversive footshock or (2) rats received footshock after injections of the muscarinic ACh receptor (mAChR) antagonist scopolamine at a dose (1 mg/kg) that disrupted long-term retention of avoidance without acutely impairing immediate avoidance or spatial tuning of place cells. Remapping after avoidance learning was similarly prevalent in subpopulations of shock-responsive and non-responsive place cells, and in contrast with some prior findings (Mamad et al., 2019), remapping did not alter the spatial distribution of place fields on the maze (i.e., there was no net migration of place fields toward or away from the shocked location). These findings add to a large body of evidence showing that place cell remapping occurs in response to aversive events, and also provide new evidence that remapping occurs preferentially under conditions where aversive encounters are remembered rather than forgotten, consistent with the hypothesis that place cell remapping may play a role in storing memories of aversive encounters. Results Male (n = 7) and female (n = 8) Long–Evans rats underwent survival surgery to inject 1.2 uL of AAV9-Syn-GCamp7s (AddGene) in the hippocampal CA1 layer; ~2 wk later, a 1.8-mm-diameter GRIN lens stack (~0.5 pitch) was unilaterally implanted to image CA1 neurons. A baseplate was attached to the skull for mounting the miniscope, and then rats began a regimen of running one 15 min session per 48 hr on a 250 × 125 cm rectangular maze (Figure 1A). Rats earned 20 mg chocolate pellets by alternating between two rewarded corners. On each trial, rats were free to choose a direct short path (250 cm) or an indirect long path (500 cm) to reach the next reward. During early sessions, rats learned to prefer the short over the long path (Figure 1C and D). Upon reaching criterion for short path preference (>2 rewards/min, and twice as many short paths to long paths), rats began receiving drug-free shock, scopolamine shock, or barrier training sessions (Figure 1B). Figure 1 with 1 supplement see all Download asset Open asset Disruption of aversive avoidance acquisition by scopolamine. (A) Overhead view of the rectangular maze. (B) Order of treatment for five subgroups of rats in the study. The number of sessions in ACQ and EXT boxes varied per rat, depending on how many sessions it took individual subjects to reach behavioral criteria. (C) Example trajectories from sessions 1, 3, and 5 during initial acquisition of short path preference. (D) Acquisition curves for short path preference; criterion was reached on session 0. Black lines show mean +/- 1 standard deviation for the session (E) Example maze trajectories from training sessions. (F) Left: rewards/min earned on the short path during the first 10 min (pre10) versus last 5 min (post5) of training sessions; symbols indicate whether each rat received its first (shk1) or second (shk2) shock during a session. Right: boxplots show post-shock reduction in short path rewards/min (post5/pre10). (G) Example maze trajectories 48 hr after training. (H) Left: rewards/min earned on the short path during drug-free sessions given 48 hr before (–48 hr) vs. after (+48 hr) training. Right: boxplots show 48 hr retention of shock avoidance (+48 hr/ –48 hr). (I) Example maze trajectories 144 hr after training. (J) Left: extinction curves over the first three post-extinction sessions; number of rewards earned on the short path is measured as a percentage of baseline (48 hr before training; thin lines: individual rats, thick lines: per session median). Right: cumulative distributions show percentage of rats in each training condition meeting extinction criterion (≥2 rewards/min on the short path, and at least twice as many short path rewards as long path rewards) at 1, 2, 3, or 4 d after training. *p<0.05, **p<0.01, ****p<0.0001. Acquisition and extinction of avoidance learning During shock training sessions (drug-free or scopolamine), rats performed the standard alternation task for 10 min. Then a 1.0 mA scrambled current was switched on to electrify grid bars in a 50 cm segment of the short path’s center (Figure 1A). Identical grid bars spanned the full length of the long and short paths, so there were no local cues to indicate the shock zone’s location. After encountering the shock zone 1–2 times, rats subsequently avoided the short path during the final 5 min of the session (Figure 1E). In the scopolamine shock condition, lens-implanted rats received 1.0 mg/kg scopolamine via intraperitoneal injection 30 min prior to the start of the shock session. In the drug-free condition, lens-implanted rats received no injection prior to the start of the shock session. To control for effects of the injection procedure, a separate cohort of rats without lens implants was given injections of saline or scopolamine prior to shock training; in animals without lens implants, scopolamine-injected rats showed impaired avoidance learning compared with saline-injected rats that was similar to the impairment seen between scopolamine-injected and drug-free (non-injected) rats with lens implants (Figure 1—figure supplement 1B and C), indicating that the injection procedure itself was not responsible for effects induced by scopolamine. In the barrier control condition, the maze was not electrified; instead, a clear plexiglass barrier was placed in the center of the short path, forcing the rat to take the long path during the final 5 min of the session. During the first 10 m of training on scopolamine (before shock delivery), 6/10 rats (three males, three females) fell below the criterion for preferring the short path (compared with 0/14 drug-free rats). These rats earned a median of five short path rewards/min during the drug-free session given 48 hr before training, but only 1.9 short path rewards/min during the first 10 min (before shock) of their training session on scopolamine (Figure 1F, ‘scopolamine shock pre10’; Wilcoxon test, p=0.0098). Thus, prior to shock delivery, scopolamine impaired expression of the rats’ learned preference for taking the short path (Figure 1E, middle). During the training session, rats earned fewer rewards/min on the short path after than before grid electrification (Figure 1F) in both the drug-free (n = 14, signed-rank test, p=1.2e-4) and scopolamine (n = 10, signed-rank test, p=0.004) conditions. Rats in the barrier condition (n = 6) were likewise forced to stop taking the short path after it was blocked by the barrier (Figure 1F, left panel). Rats in the drug-free shock condition showed long-term retention of avoidance (Figure 1G, left), earning fewer rewards/min on the short path 48 hr after than 48 hr before training (Figure 1H, Wilcoxon test, p=3.7e-4). By contrast, most rats trained on scopolamine showed similar short path reward rates during drug-free sessions given 48 hr before and after training (Figure 1H, Wilcoxon test, p=0.125), and thus failed to exhibit long-term retention of avoidance (Figure 1G, middle). When tested 48 hr after training, rats shocked on scopolamine showed less avoidance of the short path than rats shocked drug-free (rank-sum test: p=0.0235; Figure 1H). Hence, pre-training scopolamine injections impaired aversive learning, consistent with prior studies (Decker et al., 1990; Anagnostaras et al., 1999; Green et al., 2005). Between- versus within-session place cell stability A large-field-of-view version of the UCLA Miniscope (‘MiniLFOV’; Guo et al., 2023) was used to image neurons in the hippocampal CA1 layer through the implanted GRIN lens during maze sessions (Figure 2A). Although the GRIN lens caused some flattening and compression of stratum oriens (Figure 2—figure supplement 1), this did not appear to cause significant disruptions of CA1 activity since spatial tuning properties of place cells were stable and intact (see below). Figure 2 with 8 supplements see all Download asset Open asset Between- versus within-session population coding. (A) Upper left: illustration of rat wearing MiniLFOV. Upper right: cell contours identified during pre-training (green) and training (red) sessions in one rat; regions of overlap between contours that recurred in both sessions appear yellow. Lower left: target position of GRIN lens over the CA1 layer. Lower right: fluorescence image of lens position from the example rat. (B) Top: rastergram shows normalized calcium fluorescence traces of place cells (one per row, sorted by preferred firing location and direction) during several traversals of the short path during an example session. Bottom: rat’s position (black) with running epochs colored by direction of travel (‘LR,’ left to right, in blue; ‘RL,’ right to left, in red). (C) Individual rat data (lines and symbols) and session means (bars) for the number of subsampled beeline trials (left) and median beeline running speed (right) during pre-training (pre) and training (trn) sessions; subsampled beeline trial counts were lower for trn than pre sessions because only trials from the first 10 min of trn (prior to shock delivery) were included; running speeds were lower for trn than pre sessions because scopolamine (SCP) reduced running speeds, resulting in preferential subsampling of slower beeline trials from drug-free (DF) sessions by the algorithm that minimized running speed differences between training conditions (see ‘Methods’). (D) Bar/line graphs show number of place cells imaged per rat (left) and percentage of all imaged cells classified as place cells (right) during pre and trn sessions. (E) Pie graphs show percentages of place cells imaged per condition (‘n’ gives total number summed over rats) that were spatially tuned in the LR only, RL only, or both LR and RL running directions. (F) Tuning curve properties of place cells imaged during pre and trn sessions. (G) Place cell recurrence ratios (RR) between pre and trn sessions. (H) Top: diagram shows timeline for pre and trn sessions given 48 hr apart. Bottom: tuning curve heatmaps for recurring place cells (from all rats combined, co-sorted by peak locations from the trn1 session) that were spatially tuned in the LR (top) or RL (bottom) running directions; separate heatmaps are shown for pre, trn part 1 (trn1), and trn part 2 (trn2) sessions. (I) Between- (B) and within- (W) session population vector correlation matrices are shown for DF and SCP shock training conditions; middle bar graph shows median place tuning stability (S) for each rat (lines and symbols) and mean over rats (bars) for B and W heatmap pairs. Asterisks in (C) and (D) denote significance for main effect of DF vs. SCP or uncorrected t-test comparing pre vs. trn sessions; asterisks in (E) and (G) denote significance for uncorrected t-tests. †p<0.1; *p<0.05; **p<0.01; ***p<0.001. Calcium activity was analyzed only during traversals of the short path since the long path was undersampled after rats had learned to prefer the short path. Analysis was further restricted to beeline trials during which the rat ran directly from one reward zone to the other on the short path, without any pause or change in direction (Figure 2B, Video 1); this assured that imaging data came from periods of active locomotion when place cells exhibit reliable spatial tuning, and that the rats’ behavior during imaging was similar across all experimental sessions and conditions. To further control for possible confounding effects of behavior differences between sessions (see Figure 2—figure supplement 2), beeline trials were randomly subsampled using an algorithm (see ‘Methods’) that minimized trial count and running speed differences between the drug-free and scopolamine conditions (Figure 2C). Spatial tuning was then analyzed and compared during these behaviorally homogeneous trials. To analyze spatial tuning, the short path was subdivided into 23 spatial bins (each 10.8 cm wide). Two spatial tuning curves (one per running direction) were derived for each neuron. Cell activity was measured in units of active frames per second (Af/s), defined as the mean number of imaging frames per second during which a neuron generated at least one inferred spike. A neuron was classified as a place cell if its LR or RL tuning curve (or both) met defined criteria for minimum Af/s, spatial selectivity, and spatial stability within a session (see ‘Methods’). About 1/3 of place cell tuning curves met the criteria for spatial selectivity only in the LR direction, 1/3 only in the RL direction, and 1/3 in both directions (Figure 2E). It should be noted that since we used a ubiquitous synapsin promoter to drive expression of GcaMP7s, some neurons classified as place cells might have been CA1 interneurons rather than pyramidal cells. Video 1 Download asset This video cannot be played in place because your browser does support HTML5 video. You may still download the video for offline viewing. Download as MPEG-4 Download as WebM Download as Ogg Video demonstrating behavior and calcium imaging recorded from one rat performing linear alternation along the short path of the maze. (A) Position of the rat (red dot). (B) Motion-corrected video of calcium fluorescence. (C) Processed demixed/denoised CaImAn output (spatial contours modulated by denoised calcium trace). (D) Right half shows calcium activity of 290 identified neurons in the video, sorted by their preferred firing direction (teal/pink) and location along the track. Current time highlighted in the center gray region. To analyze acute effects of scopolamine on CA1 place cell activity, data from drug-free or scopolamine shock sessions was compared against data from pre-training baseline sessions (always drug-free) given 48 hr earlier. The drug-free condition only included rats (n = 9) that retained avoidance of the short path 48 hr aftershock training, whereas the scopolamine condition only included rats (n = 7) that failed to avoid the short path 48 hr aftershock training (indicating that the drug had blocked avoidance learning). A 2 × 2 ANOVA on the number of place cells detected per session (Figure 2D, left) found no effect of training condition (F1,14 = 0.03, p=0.87) or session (F1,14 = 0.014, p=0.92), and no interaction (F1,14 = 2.1, p=0.17). A similar ANOVA on the percentage of imaged cells per session that were classified as place cells (Figure 2D, right) found no effect of training condition (F1,14 = 0.07, p=0.79), but place cell percentages were lower during training than pre-training sessions (F1,14 = 5.1, p=0.04); this reduction was greater in the scopolamine than drug-free condition, resulting in a marginal interaction effect (F1,14 = 4.4, p=0.0539). An analysis of how spatial tuning varied with the size and location of cell contours revealed that contours of non-place cells tended to be slightly but significantly smaller (p<0.01) and nearer to the lens center (p<0.05) than contours of place cells (Figure 2—figure supplement 3A). For tuning curves that met the criteria for spatial selectivity in each session, four tuning properties were analyzed: peak Af/s rate, out-of-field Af/s rate, tuning width, and spatial information content (see ‘Methods’). For each rat and each session, median values of these tuning properties were taken over all LR and RL tuning curves that met spatial selectivity criteria (Figure 2—figure supplement 4); 2 × 2 mixed ANOVAs were then performed on the resulting rate medians for each of the four tuning properties (Figure 2F). There were large main effects of session (pre-training vs. training) for all four tuning properties, which were driven by correspondingly large differences in behavior sampling and running speed (Figure 2C). However, there were no main effects of training condition (drug-free vs. scopolamine) or interactions between training condition and session (Figure 2F), indicating that none of the four tuning properties differed during training sessions given drug-free versus on scopolamine. The place field recurrence ratio was defined as RR=NR/NT , where NR is the number of place fields that recurred during the pre-training and training sessions, and NT is the total number of recurring and non-recurring place fields detected during both sessions combined (see ‘Methods’). Mean RR values were lower (independent t14=2.15, p=0.0497) during scopolamine (40.7 ± 8.8%) than drug-free (50.7 ± 3.9%) training sessions, consistent with the findings reported above that the proportion of neurons classified as place cells during the training session was lower on scopolamine than drug-free (Figure 2D, right). It was observed that contours of recurring place cells tended to be slightly but significantly smaller (p<0.01) and nearer to the lens center (p<0.01) than contours of non-recurring place cells (see Figure 2—figure supplement 3B and C). To investigate how scopolamine affected population coding by recurring place cells, two heatmaps (one per running direction, denoted HLRpre and HRLpre) were created from pre-training tuning curves of recurring place cells (Figure 2H, Figure 2—figure supplement 5). Additionally, two heatmaps per running direction were created from data collected during the first (HLRtrn1 , HRLtrn1) and second (HLRtrn2 , HRLtrn2) half of each training session’s subsampled beeline trials, all of which occurred prior to shock delivery. Between-session population vector correlation matrices (one per running direction) were derived for each rat (Figure 2—figure supplement 5) with matrix entries given by ρi,jbtwn=R(Hipre,Hjtrn1), where Hipre and Hjtrn1 denote population vectors in columns i and j of the pre-training and trn1 heatmaps, respectively, and R is the Pearson correlation coefficient. Within-session population vector correlation matrices were derived in a similar manner with matrix entries given by ρi,jwthn=R(Hitrn1,Hjtrn2), where Hitrn1 and Hjtrn2 denote population vectors in columns i and j of the trn1 and trn2 heatmaps, respectively. When population vector correlation matrices were averaged together across running directions and rats (Figure 2I), high mean ρwthn values were observed along diagonals of within-session correlation matrices for both the drug-free and scopolamine conditions. By contrast, lower mean ρbtwn values were observed along diagonals of between-session correlation matrices, in accordance with prior studies showing that place cell population vectors become decorrelated over time (Mankin et al., 2012; Ziv et al., 2013; Cai et al., 2016; Keinath et al., 2022). To quantify this decorrelation, a place tuning stability score (S) was computed as S = median(ρ1LR-ρoffLR , ρ2LR-ρoffLR ,..., ρKLR-ρoffLR , ρ1RL-ρoffRL , ρ2RL-ρoffRL ,..., ρKRL-ρoffRL), where ρoffLR and ρoffRL are mean off-diagonal ρ values and ρiLR and ρiRL are individual peri-diagonal ρ values for bins in the rat’s LR and RL correlation matrices (see ‘Methods’). A 2 × 2 mixed ANOVA on S scores with training condition (drug-free vs. scopolamine) as an independent factor and time interval (between vs. within session) as a repeated factor found no main effect of training condition (F1,14 = 1.73, p=0.21), but there was a large main effect of time interval (F1,14 = 71.5, p=7.1e-7) and a significant interaction (F1,14 = 8.1, p=0.0132). Uncorrected post hoc comparisons confirmed that this was because scopolamine injections reduced between- (t14 = 3.1, SDF < SSCP p=0.0084) but not within- (t14 = 0.83, SDF < SSCP p=0.42) session population vector correlations (Figure 2I, center). Hence, even though scopolamine did not acutely disrupt spatial tuning of CA1 neurons (Figure 2F), the drug reduced the percentage of recurring place cells and degraded the between-session (but not within-session) similarity of recurring place cell population vectors (Figure 2H and I). Similar disruption of between- but not within-session place cell stability has been previously reported in aged rats (Barnes et al., 1997). Disruption of between-session place cell stability by scopolamine was similar in male and female rats (Figure 2—figure supplement 6). Cross-session stability of population vectors was completely abolished in control analyses (see ‘Methods’) where inferred spikes were circularly shifted against position tracking data during each individual beeline trial of the pre-training reference session (Figure 2—figure supplement 7). When analyses of Figure 2 were repeated on scopolamine rats (n = 2) that retained avoidance despite the injection, population vector similarity was not degraded between pre-training and training sessions, suggesting that impairment of between-session place tuning stability was related to impairment of avoidance learning (Figure 2—figure supplement 8). When the analyses were repeated on drug-free rats (n = 2) that failed to retain avoidance despite being trained drug free, between- and within-session population vector similarity were indistinguishable from drug rats that retained avoidance (Figure 2—figure supplement 8), implying that failure to acquire avoidance in these rats was not attributable to any noticeable deficiency in the fidelity of the hippocampal place code during training. Induction of place cell remapping by aversive learning Training-induced place cell remapping was analyzed in the same subset of rats shown in Figure 2. To measure remapping, post-extinction CA1 population vectors were compared against the 48 hr pre-acquisition baseline session. For the" @default.
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W4385250143 title "Author response: Hippocampal place cell remapping occurs with memory storage of aversive experiences" @default.
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