Almut Hupbach

Memory formation, consolidation and transformation

Memory formation is a highly dynamic process. In this review we discuss traditional views of memory and offer some ideas about the nature of memory formation and transformation. We argue that memory traces are transformed over time in a number of ways, but that understanding these transformations requires careful analysis of the various representations and linkages that result from an experience. These transformations can involve: (1) the selective strengthening of only some, but not all, traces as a function of synaptic rescaling, or some other process that can result in selective survival of some traces; (2) the integration (or assimilation) of new information into existing knowledge stores; (3) the establishment of new linkages within existing knowledge stores; and (4) the up-dating of an existing episodic memory. We relate these ideas to our own work on reconsolidation to provide some grounding to our speculations that we hope will spark some new thinking in an area that is in need of transformation.

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.

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.

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.

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.

Spatial Reorientation: Effects of Verbal and Spatial Shadowing

ABSTRACT Spatially disoriented adults flexibly conjoin geometric information (macroscopic shape) and nongeometric information (e.g., the color of a wall) to re-establish their bearings. It has been proposed that non-geometric information is incorporated into a geometric frame of reference through the use of spatial language. Support for this assumption comes from dual-task studies in which participants failed to use non-geometric features when they shadowed a verbal message concurrent to the reorientation task. These studies were performed in small rectangular spaces. In contrast, our study was performed in a large square room. Experiment 1 showed that verbal shadowing did not disrupt non-geometric feature use in this environment. In Experiment 2, we found that a spatial shadowing task that required the encoding of frequently changing spatial directions impaired reorientation behavior. Our study shows that nongeometric information can be used for reorientation without recourse to linguistic processes, and suggests that the use of non-geometric features is dependent upon a spatial coding process.

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

HighlightsMeta‐analyses revealed reliable reconsolidation effects for episodic memories.Reactivation makes episodic memories susceptible to physiological and behavioral interference.Effects are more pronounced for remote memories and memories of narrative structure.New information presented after reactivation intrudes into the original memory.Findings support a dynamic view of long‐term memory. Abstract 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.

Effects of psychosocial stress on episodic memory updating

RationaleWhen 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.MethodsParticipants 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).ResultsMemory 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.ConclusionThe 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.

The Specific Outcomes of Reactivation-Induced Memory Changes Depend on the Degree of Competition between Old and New Information

cific type of memory alteration (impair-ment, extinction, incorporation of new information) is dependent upon the relative localization vs. distribution of the underlying memory representations. Fear conditioning and procedural memory are supported by rather localized brain systems (fear condition-ing: basolateral amygdala, e.g., LeDoux, 2000; motor sequence learning: basal ganglia, e.g., Packard and Knowlton, 2002). In contrast, episodic memories depend on the interplay between the hippocampal proper and wide-spread neocortical areas (see, e.g., Dickerson and Eichenbaum, 2010 , for a review). Schiller and Phelps propose the following principle: the more localized a representation, the more likely behavioral interference will cause mem-ory impairment; whereas, the more distrib-uted the underlying memory representations, the more likely will behavioral interference result in integration of the new information into the reactivated memory.I suggest an alternative explanation of the different outcomes in the differ-ent paradigms used. I would like to argue that the reviewed studies do not only dif-fer with respect to the relative localization vs. distribution of brain systems involved, but also with respect to how the potentially interfering material that is presented after reactivation relates to the content of the original memory that reactivation renders labile. More specifically, although all of the reviewed studies use behavioral interference paradigms, the studies differ in the degree with which the newly presented informa-tion competes with the previously encoded information. In fear conditioning, the new information (“no shock”) is in direct com-petition with the previously learned contin-gency (“shock”), i.e., an organism cannot display both responses simultaneously (fear and no fear; although, interestingly, there is a dissociation between the physi-ological response and explicit knowledge of the contingency). In procedural memory,

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.