The effects of variable encoding contexts on item and source recognition.

How repeated encoding affects retention of item details is an unresolved question. The Competitive Trace theory (Yassa & Reagh, Frontiers in Behavioral Neuroscience, 7, 107, 2013) assumes that even slight variations in encoding contexts across item repetitions induce competition among non-overlapping contextual traces, leading to semanticization and decontextualized memory traces. However, empirical support for this assumption is mixed. In extension of previous research, the current study attempted to increase the competition between contextual traces by increasing encoding context variability. In three experiments we tested how repeated encoding in the same context or different contexts affects target recognition, similar lure discrimination, and source memory. Participants viewed images of objects once, three times in the same or three times in different contexts. Context variability was implemented through variations in background color or encoding tasks. Repeated encoding improved memory for item details, independent of context variability. Background color was poorly remembered but answering different encoding questions for repeated items impaired recollection of specific encoding tasks, in comparison to encoding items only once or repeatedly with the same encoding task. Our findings show that repetitions enhance memory for perceptual details but can impair memory for contextual elements, a dissociation that needs to be considered by the Competitive Trace Theory and other consolidation theories.

Repeated encoding fosters retention of perceptual detail in visual recognition memory.

In a 2014 issue of Learning & Memory, Reagh and Yassa proposed that repeated encoding leads to semanticization and loss of perceptual detail in memory. We presented object images one or three times and tested recognition of targets and corresponding similar lures. Correct lure rejections after one in comparison to three exposures were more frequently associated with corresponding target misses, suggesting that higher lure rejections after one exposure reflect memory failure rather than perceptual fidelity. Signal detection theory analysis showed that three exposures improved lure-old discriminations. Thus, repeated encoding fosters rather than hinders retention of perceptual detail in visual recognition memory.

Stress-Induced Increase in Cortisol Negatively Affects the Consolidation of Contextual Elements of Episodic Memories.

Stress can modulate episodic memory in various ways. The present study asks how post-encoding stress affects visual context memory. Participants encoded object images centrally positioned on background scenes. After encoding, they were either exposed to cold pressure stress (CPS) or a warm water control procedure. Forty-right hours later, participants were cued with object images, and for each image, they were asked to select the background scene with which it was paired during study among three highly similar options. Only male but not female participants reacted with a significant increase in salivary cortisol to CPS, and the stress and control group did not differ in recognition performance. Comparing recognition performance between stress responders and non-responders, however, revealed a significant impairment in context memory in responders. Additionally, proportional increase in cortisol was negatively correlated with the number of correctly recognized scenes in responders. Due to the small number of responders, these findings need to be interpreted with caution but provide preliminary evidence that stress-induced cortisol increase negatively affects the consolidation of contextual elements of episodic memories.

Different reactivation procedures enable or prevent episodic memory updating.

The present study asked whether the specific method of reactivation modulates the impact of new learning on reactivated episodic memories. The study consisted of three sessions that were spaced 48 hr apart. It used an ABAC paradigm that allowed for the simultaneous assessment of retroactive interference (RI: reduced A-B recall after A-C learning) and intrusions from C into A-B recall. In Session 1, participants learned a list of paired-associates A-B. In Session 2, memory for A-B was reactivated or not and then participants either learned a second list of paired-associates A-C or completed a control task. Three different reminder conditions were compared to a no-reminder condition: a test condition, in which participants were asked to recall B in response to A, a restudy condition, in which A-B pairs were presented again for study, and a cue-word only reminder condition, in which A cues were presented in an unrelated rating task. In Session 3, recall of A-B was tested. Moderate or indirect reactivation of A-B (presentation of cue-words only) resulted in high RI effects and intrusion rates, whereas strong and direct reactivation (test and restudy) drastically reduced these effects. We suggest that direct reactivation of A-B before A-C learning strengthens memory and draws attention to list differences, thereby enhancing list segregation, and reducing memory updating.

Differential effects of unipolar versus bipolar depression on episodic memory updating.

Episodic memories, when reactivated, can be modified or updated by new learning. Since such dynamic memory processes remain largely unexplored in psychiatric disorders, we examined the impact of depression on episodic memory updating. Unipolar and bipolar depression patients, and age/education matched controls, first learned a set of objects (List-1). Two days later, participants in all three groups were either reminded of the first learning session or not followed by the learning of a new set of objects (List-2). Forty-eight hours later, List-1 recall was impaired in unipolar and bipolar patients compared to control participants. Further, as expected, control participants who received a reminder spontaneously recalled items from List-2 during recall of List-1, indicative of an updated List-1 memory. Such spontaneous intrusions were also seen in the unipolar and bipolar patients that received the reminder, suggesting that memory updating was unaffected in these two patient groups despite impaired recall of List 1. Unexpectedly, we observed a trend towards higher intrusions, albeit statistically insignificant, not only in the reminder but also in the no-reminder subgroups of bipolar patients. We probed this further in a second cohort by testing recall of List-2, which was also impaired in both depression groups. Again bipolar patients showed intrusions, but this time in the reverse order from List-1 into List-2, independent of a reminder. Taken together, despite impaired recall, updating of episodic memories was intact and unidirectional in unipolar depression. In contrast, indiscriminate updating, as evidenced by bidirectional interference between episodic memories, was seen in bipolar depression. These findings reveal a novel distinction between unipolar versus bipolar depression using a reactivation-dependent memory updating paradigm.

Long-term effects of directed forgetting.

The intention to forget reduces the accessibility of information in memory, which is commonly explained with temporary retrieval difficulties. Long-term effects have rarely been studied, and results are inconsistent. The present study re-assessed the long-term effects of directed forgetting (DF). Participants encoded a first list of items (L1), and were then instructed to forget or to remember this list. Immediately afterwards, all participants were presented with a second list to remember. In Experiment 1, memory for L1 and L2 was assessed after a 24-h delay. The forget cue reduced the number of items that were recalled from L1. Experiment 2 implemented a 12-h delay between encoding and test that was either filled with day-time wakefulness or night-time sleep. Replicating the findings of Exp. 1, recall of L1 was reduced in the forget in comparison to the remember condition. Sleep in comparison to wakefulness significantly strengthened L1 memory in the remember group only. Taken together, the present study shows that the intention to forget can have long-lasting consequences. This suggests that different mechanisms underlie the short- and long-term effects of DF, with long-term effects potentially reflecting the preferential consolidation of information that has been identified as important during encoding.

Does reactivation trigger episodic memory change? A meta-analysis.

According to the reconsolidation hypothesis, long-term memories return to a plastic state upon their reactivation, leaving them vulnerable to interference effects and requiring re-storage processes or else these memories might be permanently lost. The present study used a meta-analytic approach to critically evaluate the evidence for reactivation-induced changes in human episodic memory. Results indicated that reactivation makes episodic memories susceptible to physiological and behavioral interference. When applied shortly after reactivation, interference manipulations altered the amount of information that could be retrieved from the original learning event. This effect was more pronounced for remote memories and memories of narrative structure. Additionally, new learning following reactivation reliably increased the number of intrusions from new information into the original memory. These findings support a dynamic view of long-term memory by showing that memories can be changed long after they were acquired.

Stress selectively affects the reactivated components of a declarative memory.

When long-term memories are reactivated, they can reenter a transient plastic state in which they are vulnerable to interference or physiological manipulations. The present study attempted to directly affect reactivated memories through a stress manipulation, and compared the effects of stress on reactivated and nonreactivated components of a declarative memory in a within-subject design. We presented image pairs that consisted of an image of an animal and an image of an unrelated object. Participants were instructed to memorize the object images. Forty-eight hours later, we presented half of the animal images again in an unrelated task to indirectly reactivate the associated object images. Immediately after reactivation, participants were exposed to cold pressor stress or a warm water control condition. Forty-eight hours later, we assessed memory for the object images with a free recall test. Reactivation boosted memory performance in the control condition, such that reactivated items were better recalled than nonreactivated items. This memory-enhancing effect of reactivation was completely abolished by cold pressor stress. Importantly, stress selectively impacted only the reactivated items while leaving memory for the nonreactivated items unaffected. The present study shows that it is possible to selectively reactivate and modulate specific parts of a declarative memory.

Memory for emotionally arousing items: context preexposure enhances subsequent context-item binding.

Emotionally arousing events are better remembered than neutral events. Not all components of these events, however, are equally well remembered and bound in memory. Although arousal enhances memory for central information, it tends to impair memory for peripheral details, referred to as central/peripheral trade-off. Therefore, people often have difficulties remembering which emotional stimuli were encountered in which contexts. The present study asked whether such context-item binding could be enhanced when individuals are familiarized with context images that later serve as background cues for emotionally arousing stimuli. Familiarization allows for context encoding prior to the encounter of emotionally arousing stimuli. Thus, only few attentional or cognitive resources may be required for context encoding when the arousing stimuli are presented, which might then allow for more efficient context-item binding. In line with this hypothesis, we show that context-item binding significantly improved under these conditions for emotionally negative stimuli. Our results suggest that context familiarity promotes context-item binding for emotional events.

Additional boundary condition for list-method directed forgetting: the effect of presentation format.

The attempt to forget some recently encoded information renders this information difficult to recall in a subsequent memory test. "Forget" instructions are only effective when followed by learning of new material. In the present study, we asked whether the new material needs to match the format of the to-be-forgotten information for forgetting effects to emerge. Participants studied visually presented words or line drawings (L1) and afterward were instructed to remember or forget these items. Then a 2nd conceptually unrelated list (L2) was presented that either matched or mismatched the format of L1. Forgetting effects were observed only when the lists matched in format but not when the formats mismatched. This result establishes an important boundary condition of directed forgetting and suggests that when salient retrieval cues guide retrieval, they eliminate the effect of the "forget" cue. Implications for theories of directed forgetting are discussed.

Neural context reinstatement predicts memory misattribution.

What causes new information to be mistakenly attributed to an old experience? Some theories predict that reinstating the context of a prior experience allows new information to be bound to that context, leading to source memory confusion. To examine this prediction, we had human participants study two lists of items (visual objects) on separate days while undergoing functional magnetic resonance imaging. List 1 items were accompanied by a stream of scene images during the intertrial interval, but list 2 items were not. As in prior work by Hupbach et al. (2009), we observed an asymmetric pattern of misattributions on a subsequent source memory test: participants showed a strong tendency to misattribute list 2 items to list 1 but not vice versa. We hypothesized that these memory errors were due to participants reinstating the list 1 context during list 2. To test this hypothesis, we used a pattern classifier to measure scene-related neural activity during list 2 study. Because scenes were visually present during list 1 but not list 2, scene-related activity during list 2 study can be used as a time-varying neural indicator of how much participants were reinstating the list 1 context during list 2 study. In keeping with our hypothesis, we found that prestimulus scene activation during the study of list 2 items was significantly higher for items subsequently misattributed to list 1 than for items subsequently correctly attributed to list 2. We conclude by discussing how these findings relate to theories of memory reconsolidation.

When forgetting preserves memory.

There has been a resurgence of interest in defining the circumstances leading to memory modifications. Studies have shown that reactivating a supposedly stable memory re-introduces a time-limited window of plasticity during which presentation of interfering material can cause long-term memory changes. The present study asks whether such memory changes can be prevented if people are instructed to forget the memory before the new material is encoded. Participants learned a set of objects. After 48 h, they were reminded of this learning episode, and learned another set of objects. Again 48 h later, they recalled the first (Exp. 1) or second set (Exp. 3). As shown previously, a reminder caused intrusions from the second set into recall of the first set. Here I show that the instruction to forget the first set significantly diminished intrusions from the second set, especially when the instruction was given before the new set was encoded in the second session. Experiment 2 suggests that the reduced intrusions were due to list segregation/isolation, rather than temporarily inhibited access to Set 1. Taken together, the study shows that the attempt to forget a memory can immunize it such that the presentation of interfering material has limited effects, and the memory can be recalled unchanged in the future. This is important when veridical memory is essential, such as in eyewitness testimonies.

Effects of psychosocial stress on episodic memory updating.

RATIONALE: When a consolidated memory is reactivated, it becomes labile and modifiable. Recently, updating of reactivated episodic memory was demonstrated by Hupbach et al. (Learn Mem 14:47-53, 2007). Memory updating involves two vital processes-reactivation followed by reconsolidation. Here, we explored effects of psychosocial stress on episodic memory updating. Based on prior research, we hypothesized that stress before reactivation or stress before reconsolidation would impair memory updating. METHODS: Participants learned a set of objects (list 1) on day 1. On day 2, some participants were reminded of list 1 before learning a second set of objects (list 2). Memory for list 1 was tested on day 3. Stress was administered either before reactivation of list 1 on day 2 (exp 1) or before reconsolidation of list 1, i.e., after reactivation and learning list 2 on day 2 (exp 2). RESULTS: Memory updating involves the incorporation of list 2 items into list 1 memory, contingent upon the reactivation of list 1 memory. In exp 1, the reminder groups had higher intrusions than the no-reminder groups, but contrary to our predictions, stress did not reduce this reminder effect. Stress effects were, however, found in exp 2: the reminder group that was stressed after reactivation and new learning showed fewer intrusions than the control reminder group. CONCLUSION: The findings suggest that stress before reactivation does not impair memory updating but stress at the onset of reconsolidation can. Timing may determine the effects of stress on memory processing.

Moderate stress enhances immediate and delayed retrieval of educationally relevant material in healthy young men.

Retrieval practice is a powerful memory enhancer. However, in educational settings, test taking is often experienced as a stressful event. While it is known that stress can impair retrieval processes, little is known about the delayed consequences of testing memory for educationally relevant material under stressful conditions, which is the focus of the present study. Participants (38 women, 37 men) memorized a scientific text passage on Day 1. On Day 2, they were either exposed to a stressor (cold pressor test; CPS) or a warm water control, and immediately afterward, they were asked to recall the text passage (i.e., retrieval under stress vs. control). Salivary cortisol was measured as an index of the stress response before, and 20 min after the CPS versus control treatment. The delayed effects of testing under stress were assessed with a final recall test on Day 3. In comparison to the control condition, CPS caused significant increases in salivary cortisol, and, surprisingly resulted in enhanced memory in men. Importantly, this enhancement was not only observed in the test that immediately followed the stressor, but also in the delayed test. In women, CPS caused only marginal increases in cortisol concentrations, and retrieval remained unaffected. Our study suggests that moderate stress can improve memory performance for educationally relevant material in a long-lasting manner in healthy young men.

Episodic memory updating: the role of context familiarity.

We previously demonstrated that spatial context is a powerful reminder that can trigger memory updating (Hupbach, Hardt, Gomez, & Nadel in Learning & Memory, 15, 574-579 2008). In the present study, we asked whether the familiarity of the spatial context modulates the role of spatial context as a reminder. Since context familiarity can be easily manipulated in children, we chose 5-year-olds as study participants. In two experiments, we demonstrated robust memory-updating effects in children. Spatial context triggered incorporation of new information into old memories only when the context was unfamiliar. In highly familiar spatial environments (children's homes), spatial context did not initiate memory updating. Other reminders (the experimenter and a reminder question) became highly effective in familiar contexts. These findings shed further light on the specific conditions that trigger memory updating and support the view that the mechanisms underlying it are similar in children and adults.

Metyrapone administration reduces the strength of an emotional memory trace in a long-lasting manner.

CONTEXT: It has recently been demonstrated that the process of memory retrieval serves as a reactivation mechanism whereby the memory trace that is reactivated during retrieval is once again sensitive to modifications by environmental or pharmacological manipulations. Recent studies have shown that glucocorticoids (GCs) have the capacity to modulate the process of memory retrieval. This suggests that GCs could be an interesting avenue to investigate with regard to reduction of emotional memory. OBJECTIVE: The current study assessed whether a pharmacological decrease in GC levels, induced by metyrapone, a potent inhibitor of GC secretion, would affect retrieval of emotional and neutral information in an acute and/or long-lasting manner. DESIGN, SETTING, PARTICIPANTS, AND INTERVENTION: To do so, 1 × 750 mg dose of metyrapone, 2 × 750 mg dose of metyrapone, or placebo was administered to young normal participants 3 d after the encoding of a slide show having neutral and emotional segments. The experiment took place in a university and a hospital setting. MAIN OUTCOME MEASURE: Memory performance was assessed after treatment and 4 d later. RESULTS: RESULTS showed that retrieval of emotional information was acutely impaired in the double-dose metyrapone group and that this effect was still present 4 d later, when GC levels were not different between groups. CONCLUSIONS: These results show that decreasing GC levels via metyrapone administration is an efficient way to reduce the strength of an emotional memory in a long-lasting manner.

Nap-dependent learning in infants.

Sleep has been shown to aid a variety of learning and memory processes in adults (Stickgold, 2005). Recently, we showed that infants' learning also benefits from subsequent sleep such that infants who nap are able to abstract the general grammatical pattern of a briefly presented artificial language (Gomez, Bootzin & Nadel, 2006). In the present study, we demonstrate, for the first time, long-term effects of sleep on memory for an artificial language. Fifteen-month-old infants who had napped within 4 hours of language exposure remembered the general grammatical pattern of the language 24 hours later. In contrast, infants who had not napped shortly after being familiarized with the language showed no evidence of remembering anything about the language. Our findings support the view that infants' frequent napping plays an essential role in establishing long-term memory.

Episodic memory reconsolidation: updating or source confusion?

Reactivation of apparently stable, long-term memory can render it fragile, and dependent on a re-stabilisation process referred to as "reconsolidation". Recently we provided the first demonstration of reconsolidation effects in human episodic memory (Hupbach, Gomez, Hardt, & Nadel, 2007; Hupbach, Hardt, Gomez, & Nadel, 2008). Memory for a set of objects was modified by the presentation of a new set, if and only if participants were reminded of the first learning episode before learning the new set. The present study asks whether this effect can be interpreted as a source discrimination problem; i.e., participants have difficulties remembering which objects were presented during which session, and do not actually incorporate new objects into the reactivated memory. The present study used a recognition test and asked participants directly about the source of their memories. Participants in the no-reminder group showed very few source errors. Participants in the reminder group misattributed the source of objects from the second set as being from the first set but not vice versa, thus demonstrating updating of the original memory. This finding is informative with respect to the misinformation paradigm, and reconsolidation is discussed as a possible mechanism underlying our results and the misinformation effect.