Emotional Arousal and Memory Binding: An Object-Based Framework

ABSTRACT— Binding various features of an event together and maintaining these connections in memory is an essential component of episodic memories. Previous theories make contradictory predictions about the effects of emotional arousal on memory binding. In this article, I review evidence for both arousal-impaired and arousal-enhanced memory binding and explain these contradictory findings using an object-based framework. According to this framework, emotionally arousing objects attract attention that enhances binding of their constituent features. In contrast, the emotional arousal associated with one object either impairs or has no effect on the associations between that object and other distinct objects or background contextual information. After initial encoding, the attention-grabbing nature of emotionally arousing objects can lead to interference in working memory, making it more difficult to maintain other bound representations. These contrasting effects of arousal on memory binding should help predict which aspects of emotional memories are likely to be accurate and which aspects are likely to be misremembered.     

Visual memory decay is deterministic

After observers see an object or pattern, their visual memory of what they have seen decays slowly over time. Nearly all current theories of vision assume that decay of short-term memory occurs because visual representations are progressively and randomly corrupted as time passes. We tested this assumption using psychophysical noise-masking methods, and we found that visual memory decays in a completely deterministic fashion. This surprising finding challenges current ideas about visual memory and sets a goal for future memory research: to characterize the deterministic "forgetting function" that describes how memories decay over time.     

The differential effects of emotional salience on direct associative and relational memory during a nap

Relational memories are formed from shared components between directly learned memory associations, flexibly linking learned information to better inform future judgments. Sleep has been found to facilitate both direct associative and relational memories. However, the impact of incorporating emotionally salient information into learned material and the interaction of emotional salience and sleep in facilitating both types of memory is unknown. Participants encoded two sets of picture pairs, with either emotionally negative or neutral objects paired with neutral faces. The same objects were present in both sets, paired with two different faces across the sets. Baseline memory for these directly paired associates was tested immediately after encoding, followed by either a 90-min nap opportunity or wakefulness. Five hours after learning, a surprise test assessed relational memory, the indirect association between two faces paired with the same object during encoding, followed by a retest of direct associative memory. Overall, negative information was remembered better than neutral for directly learned pairs. A nap facilitated both preservation of direct associative memories and formation of relational memories, compared to remaining awake. Interestingly, however, this sleep benefit was observed specifically for neutral directly paired associates, while both neutral and negative relational associations benefitted from a nap. Finally, REM sleep played opposing roles in neutral direct and relational associative memory formation, with more REM sleep leading to forgetting of direct associations but promoting relational associations, suggesting that, while not benefitting memory consolidation for directly learned details, REM sleep may foster the memory reorganization needed for relational memory.     

Source misattributions may increase the accuracy of source judgments

Misattribution of remembered information from one source to another is commonly associated with false memories, but we demonstrate that it also may underlie memories that accord with past events. Participants imagined drawings of objects in four different locations. For each, a drawing of a similarly shaped object was seen in the same location, a different location, or not seen. When tested on memory for objects' origin (seen/imagined) and location, more false "seen" responses, but also more correct location responses, were given to imagined objects if a similar object had been seen, versus not seen, in the same location. We argue that misattribution of feature information (e.g., shape, location) from seen objects to similar imagined ones increased false memories of seeing objects but also increased correct location memories, provided the misattributed location matched the imagined objects' location. Thus, consistent with the source-monitoring framework, imperfect source-attribution processes underlie false and true memories.     

Integrated memory for objects, places, and temporal order: evidence for episodic-like memory in mice

Human episodic memory refers to the recollection of an unique past experience in terms of what happened, and where and when it happened. Factoring out the issue of conscious recollection, episodic memory, even at the behavioral level, has been difficult to demonstrate in non-human mammals. Although, it was previously shown that rodents can associate what and when or what and where information given on unique trials, it proved to be difficult to demonstrate memory for what, where, and when simultaneously in mammals, without using extensive training procedures, which might induce semantic rather than episodic memory recall. Towards the goal of an animal model of human episodic memory we designed an three-trial object exploration task in which different versions of the novelty-preference paradigm were combined to subsume (a) object recognition memory, (b) the memory for locations in which objects were explored, and (c) the temporal order memory for object presented at distinct time points. We found that mice spent more time exploring two "old familiar" objects relative to two "recent familiar" objects, reflecting memory for what and when and concomitantly directed more exploration at a spatially displaced "old familiar" object relative to a stationary "old familiar" object, reflecting memory for what and where. These results suggest that during a single test trial the mice were able to (a) recognize previously explored objects, (b) remember the location in which particular objects were previously encountered, and (c) to discriminate the relative recency in which different objects were presented. According to the currently discussed behavioral criteria for episodic-like memory in animals, our results suggest that mice are capable to form such higher order memories.     

But I thought it was Mickey Mouse: the effects of new postevent information on 18-month-olds' memory

Two experiments examined the effects of postevent information on 18-month-olds' event memory. Experiment 1 (N=60) explored whether children's memory was reinstated when action information was eliminated from the reinstatement and only object information was introduced. Experiment 2 (N=48) examined children's recall when either (a). information about the objects' target actions was replaced with new action information or (b). the original training objects were replaced with new objects. In an elicited-imitation paradigm, children were trained to perform six target actions, watched a video reinstatement 10 weeks later, and were tested for recall 24 h after reinstatement. Two results were found. First, a video reminder eliminating action information reinstated children's memory as effectively as a video containing object and action information. Second, children were reminded of their past training when during reinstatement action information was preserved and new objects were presented but were not reminded when object information was preserved and new actions were presented.     

Comparison of neural activity that leads to true memories,false memories,and forgetting: An fMRI study of the misinformation effect

False memories can occur when people are exposed to misinformation about a past event. Of interest here are the neural mechanisms of this type of memory failure. In the present study, participants viewed photographic vignettes of common activities during an original event phase (OEP), while we monitored their brain activity using fMRI. Later, in a misinformation phase, participants viewed sentences describing the studied photographs, some of which contained information conflicting with that depicted in the photographs. One day later, participants returned for a surprise item memory recognition test for the content of the photographs. Results showed reliable creation of false memories, in that participants reported information that had been presented in the verbal misinformation but not in the photographs. Several regions were more active during the OEP for later accurate memory than for forgetting, but they were also more active for later false memories, indicating that false memories in this paradigm are not simply caused by failure to encode the original event. There was greater activation in the ventral visual stream for subsequent true memories than for subsequent false memories, however, suggesting that differences in encoding may contribute to later susceptibility to misinformation.     

Reality monitoring of physically similar and conceptually related objects

Three studies showed that information used in determining a target memory’s source may be derived not only from the target event itself, but also from other nontarget events or memories. Subjects were more likely to claim that an imagined object was perceived when it physically resembled or was conceptually related to another specific item that was actually perceived, relative to when there was no physical resemblance or semantic relation. Furthermore, error rates for imagined items increased with the number of perceived items that they resembled. However, subjects’ orienting task at encoding (perceptually biased or perceptually plus conceptually biased) did not systematically affect error rates. The results indicate that reality monitoring decisions about a target object are influenced by similar physical and conceptual information that was derived from other objects.     

Incidental and intentional visual memory: What memories are and are not affected by encoding tasks?

Prior research into the impact of encoding tasks on visual memory (Castelhano & Henderson, 2005) indicated that incidental and intentional encoding tasks led to similar memory performance. The current study investigated whether different encoding tasks impacted visual memories equally for all types of objects in a conjunction search (e.g., targets, colour distractors, object category distractors, or distractors unrelated to the target). In sequences of pictures, participants searched for prespecified targets (e.g., green apple; Experiment 1), memorized all objects (Experiment 2), searched for specified targets while memorizing all objects (Experiment 3), searched for postidentified targets (Experiment 4), or memorized all objects with one object prespecified (Experiment 5). Encoding task significantly improved visual memory for targets and led to worse memory for unrelated distractors, but did not influence visual memory of distractors that were related to the target's colour or object category. The differential influence of encoding task indicates that the relative importance of the object both positively and negatively influences the memory retained.     

The use of recognition information and additional cues in inferences from memory

Goldstein and Gigerenzer's (2002) "Recognition Heuristic" (RH) was tested for its empirical validity in an experimental paradigm with induced recognition of objects. RH claims that upon inferring which of two objects (e.g., cities) scores higher on a criterion (e.g., city size), a recognized object will be chosen over an unrecognized one, if the recognition is a valid predictor of the criterion without considering additional object information. Trying to avoid potential shortcomings of former studies, we (a) used the city population task, (b) provided additional cue information only for recognized cities, and (c) had participants draw inferences from memory. Participants learned city names and additional information about some cities. They also learned that recognition and the additional information were valid predictors of the criterion "city size". In a subsequent decision phase, the additional information about the cities in memory strongly affected the inferences, suggesting that recognition information is clearly integrated into judgments, but by no means in a non-compensatory fashion that would dominate every other cue.     

The mental wormhole: Internal attention shifts without regard for distance

Attention operates perceptually on items in the environment, and internally on objects in visuospatial working memory. In the present study, we investigated whether spatial and temporal constraints affecting endogenous perceptual attention extend to internal attention. A retro-cue paradigm in which a cue is presented beyond the range of iconic memory and after stimulus encoding was used to manipulate shifts of internal attention. Participants?? memories were tested for colored circles (Experiments 1, 2, 3a, 4) or for novel shapes (Experiment 3b) and their locations within an array. In these experiments, the time to shift internal attention (Experiments 1 and 3) and the eccentricity of encoded objects (Experiments 2?C4) were manipulated. Our data showed that, unlike endogenous perceptual attention, internal shifts of attention are not modulated by stimulus eccentricity. Across several timing parameters and stimuli, we found that shifts of internal attention require a minimum quantal amount of time regardless of the object eccentricity at encoding. Our findings are consistent with the view that internal attention operates on objects whose spatial information is represented in relative terms. Although endogenous perceptual attention abides by the laws of space and time, internal attention can shift across spatial representations without regard for physical distance.     

Sequential versus simultaneous viewing of an environment: Effects of focal attention to individual object locations on visual spatial learning

We investigated memories of room-sized spatial layouts learned by sequentially or simultaneously viewing objects from a stationary position. In three experiments, sequential viewing (one or two objects at a time) yielded subsequent memory performance that was equivalent or superior to simultaneous viewing of all objects, even though sequential viewing lacked direct access to the entire layout. This finding was replicated by replacing sequential viewing with directed viewing in which all objects were presented simultaneously and participants’ attention was externally focused on each object sequentially, indicating that the advantage of sequential viewing over simultaneous viewing may have originated from focal attention to individual object locations. These results suggest that memory representation of object-to-object relations can be constructed efficiently by encoding each object location separately, when those locations are defined within a single spatial reference system. These findings highlight the importance of considering object presentation procedures when studying spatial learning mechanisms.     

Prime time news: The influence of primed positive and negative emotion on susceptibility to false memories

We examined the relation between emotion and susceptibility to misinformation using a novel paradigm, the ambiguous stimuli affective priming (ASAP) paradigm. Participants (N = 88) viewed ambiguous neutral images primed either at encoding or retrieval to be interpreted as either highly positive or negative (or neutral/not primed). After viewing the images, they either were asked misleading or non-leading questions. Following a delay, memory accuracy for the original images was assessed. Results indicated that any emotional priming at encoding led to a higher susceptibility to misinformation relative to priming at recall. In particular, inducing a negative interpretation of the image at encoding led to an increased susceptibility of false memories for major misinformation (an entire object not actually present in the scene). In contrast, this pattern was reversed when priming was used at recall; a negative reinterpretation of the image decreased memory distortion relative to unprimed images. These findings suggest that, with precise experimental control, the experience of emotion at event encoding, in particular, is implicated in false memory susceptibility.     

Adult age differences in memory for schema-consistent and schema-inconsistent objects in a real-world setting

The present study examined age-related differences in the inconsistency effect, in which memory is enhanced for schema-inconsistent information compared to schema-consistent information. Young and older adults studied schema-consistent and schema-inconsistent objects in an academic office under either intentional or incidental encoding instructions, and were given two recognition tests either immediately or after 48 hr: A yes/no item recognition test that included modified remember/know judgments and a token recognition test that required determining whether an original object was replaced with a different object with the same name. Young and older adults showed equivalent inconsistency effects in both item and token recognition tests, although older adults reported phenomenologically less rich memories of schema-inconsistent objects relative to young adults. These findings run counter to previous reports suggesting that aging is associated with processing declines at encoding that impair memory for details of schema-inconsistent or distinctive events. The results are consistent with a retrieval-based account in which age-related difficulties in retrieving contextual details can be offset by environmental support.     

Sleep preferentially enhances memory for emotional components of scenes

ABSTRACT— Central aspects of emotional experiences are often well remembered at the expense of background details. Previous studies of such memory trade-offs have focused on memory after brief delays, but little is known about how these components of emotional memories change over time. We investigated the evolution of memory for negative scenes across 30 min, 12 daytime hours spent awake, and 12 nighttime hours including sleep. After 30 min, negative objects were well remembered at the expense of information about their backgrounds. Time spent awake led to forgetting of the entire negative scene, with memories of objects and their backgrounds decaying at similar rates. Sleep, in contrast, led to a preservation of memories of negative objects, but not their backgrounds, a result suggesting that the two components undergo differential processing during sleep. Memory for a negative scene develops differentially across time delays containing sleep and wake, with sleep selectively consolidating those aspects of memory that are of greatest value to the organism.     

False memory and importance: Can we prioritize encoding without consequence?

Given the large amount of information that we encounter, we often must prioritize what information we attempt to remember. Although critical for everyday functioning, relatively little research has focused on how people prioritize the encoding of information. Recent research has shown that people can and do selectively remember information assigned with higher, relative to lower, importance. However, the mechanisms underlying this prioritization process and the consequences of these processes are still not well understood. In the present study, we sought to better understand these prioritization processes and whether implementing these processes comes at the cost of memory accuracy, by increasing false memories. We used a modified form of the Deese/Roediger–McDermott (DRM) paradigm, in which participants studied DRM lists, with each list paired with low, medium, or high point values. In Experiment 1, encoding higher values led to more false memories than did encoding lower values, possibly because prioritizing information enhanced relational processing among high-value words. In Experiment 2, disrupting relational processing selectively reduced false memories for high-value words. Finally, in Experiment 3, facilitating relational processing selectively increased false memories for low-value words. These findings suggest that while prioritizing information can enhance true memory, this process concomitantly increases false memories. Furthermore, the mechanism underlying these prioritization processes depends on the ability to successfully engage in relational processing. Thus, how we prioritize the encoding of incoming information can come at a cost in terms of accurate memory.     

Neural activity during encoding predicts false memories created by misinformation

False memories are often demonstrated using the misinformation paradigm, in which a person's recollection of a witnessed event is altered after exposure to misinformation about the event. The neural basis of this phenomenon, however, remains unknown. We used fMRI to investigate encoding processes during the viewing of an event and misinformation to see whether neural activity during either encoding phase could predict what would be remembered. fMRI data were collected as participants studied eight vignettes (Original Event phase). Shortly afterward, participants studied the same vignettes during scanning, but with changes to several details, serving as the misinformation (Misinformation phase). Two days later, their memories for the Original Event were assessed. Activity that subsequently led to true and false memories was examined during both encoding phases. Two interaction patterns between encoding phase (Original Event and Misinformation) and type of memory (true and false) were observed in MTL and PFC regions. In the left hippocampus tail and perirhinal cortex, a predictive item-encoding pattern was observed. During the Original Event phase, activity was greater for true than false memories, whereas during the Misinformation phase, activity was greater for false than true memories. In other regions, a pattern suggestive of source encoding was observed, in which activity for false memories was greater during the Original Event phase than the Misinformation phase. Together, these results suggest that encoding processes play a critical role in determining true and false memory outcome in misinformation paradigms.     

Internal languages of retrieval: The bilingual encoding of memories for the personal past

In contrast to most research on bilingual memory that focuses on how words in either lexicon are mapped onto memory for objects and concepts, we focus on memory for events in the personal past. Using a word-cue technique in sessions devoted exclusively to one language, we found that older Hispanic immigrants who had come to the United States as adults internally retrieved autobiographical memories in Spanish for events in the country of origin and in English for events in the U.S. These participants were consistently capable of discerning whether a memory had come to them "in words" or not, reflecting the distinction between purely imagistic or conceptual memories and specifically linguistic memories. Via examination of other phenomenological features of these memories (sense of re-living, sensory detail, emotionality, and rehearsal), we conclude that the linguistic/nonlinguistic distinction is fundamental and independent of these other characteristics. Bilinguals encode and retrieve certain autobiographical memories in one or the other language according to the context of encoding, and these linguistic characteristics are stable properties of those memories over time.     

Testing emotional memories: does negative emotional significance influence the benefit received from testing?

A large body of research shows that emotionally significant stimuli are better stored in memory. One question that has received much less attention is how emotional memories are influenced by factors that influence memories after the initial encoding of stimuli. Intriguingly, several recent studies suggest that post-encoding factors do not differ in their effects on emotional and neutral memories. However, to date, only detrimental factors have been addressed. In the present study, we examined whether emotionally negative memories are differentially influenced by a well-known beneficial factor: the testing of memories. We employed a standard cued recall testing-effect paradigm where participants studied cue-target pairs for negative and neutral target pictures. In a subsequent post-encoding phase, one third of the cue-target pairs were tested and one third restudied; the remaining third served as control pairs. After one week, memory for all cue-target pairs was tested. While replicating both the testing effect and the emotional enhancement effect, no differences between negative and neutral memories in the benefits received from testing and restudying were observed. Thus, it seems to be true that post-encoding factors do not influence emotional memories in any other way than neutral memories, even when they are beneficial.