The role of the amygdala in emotional experience during retrieval of personal memories

ABSTRACT

Although the role of the amygdala in emotional memory retrieval has long been established, how such engagement varies depending on valence and retrieval context is less clearly understood. Participants retrieved personal memories associated with primarily positive, primarily negative, and mixed-valence images, pressing a button when successful. The button press divided trials into search and elaboration phases. Participants provided positivity and negativity ratings immediately following each trial, and then again in a post-retrieval survey. The relation between amygdala recruitment and emotionality exhibited a four-way interaction, with no other significant main effects or interactions. The interaction was driven by a temporal shift in the role of amygdala recruitment during retrieval of memories associated with mixed-valence images: Negativity ratings were supported more by search-related activity whereas positivity was more strongly associated with elaboration. Amygdala activity during retrieval relates to emotional experience in more complicated ways than previously understood. When participants were able to consider positive and negative aspects of the same event, amygdala recruitment during search and elaboration were associated with opposite behavioural effects. Such findings suggest that the amygdala may support distinct aspects of emotional experience for the same memory depending on when during retrieval it is recruited.     

Electrophysiological evidence for late maturation of strategic episodic retrieval processes

Improvement in source memory performance throughout development is thought to be mediated by strategic processes that facilitate the retrieval of task-relevant information. Using event-related potentials (ERPs), we examined developmental changes in these processes during adolescence. Adolescents (13-14 years) and adults (19-29 years) completed a memory exclusion task which required the discrimination between words studied in one color ('targets') and words studied in the alternative color ('non-targets') under two conditions that put different demands on strategic control. Memory accuracy improved with age and also increased with decreasing control demands in both age groups. The parietal old/new effect, an ERP correlate of recollection, was reliable for targets across conditions in both age groups. By contrast, ERP correlates of non-target recollection were present in adolescents across conditions but not in adults. This suggests that adults implemented a strategy to prioritize recollection of target information with greater success than adolescents regardless of control demands, presumably reflecting maturational differences in cognitive control. In support of this view, the ERP amplitude difference between targets and non-targets was positively correlated with a measure of working memory capacity (WMC) in adults but not in adolescents. A further age-related difference was that ERP correlates of post-retrieval processing, including late right-frontal old/new effects and late posterior negativities, were observed in adults only. Together, our data suggest protracted maturation in the strategic processes that underlie selective recollection and post-retrieval control.     

Aging and strategic retrieval processes: reducing false memories with a distinctiveness heuristic

The authors show that a strategic retrieval process--the distinctiveness heuristic--is a powerful mechanism for reducing false memories in the elderly. Individuals studied words, pictures, or both types of items and then completed a recognition test on which the studied items appeared once, whereas the new words appeared twice. After studying either pictures only or a mixture of pictures and words, both younger and older adults falsely recognized fewer repeated new words than did participants who studied words. Studying pictures provided a basis for using a distinctiveness heuristic during the recognition test: Individuals inferred that the absence of memory for picture information indicates that an item is "new."     

Retrieval of emotional memories

Long-term memories are influenced by the emotion experienced during learning as well as by the emotion experienced during memory retrieval. The present article reviews the literature addressing the effects of emotion on retrieval, focusing on the cognitive and neurological mechanisms that have been revealed. The reviewed research suggests that the amygdala, in combination with the hippocampus and prefrontal cortex, plays an important role in the retrieval of memories for emotional events. The neural regions necessary for online emotional processing also influence emotional memory retrieval, perhaps through the reexperience of emotion during the retrieval process.     

ERP evidence on the interaction between information structure and emotional salience of words

Both emotional words and words focused by information structure can capture attention. This study examined the interplay between emotional salience and information structure in modulating attentional resources in the service of integrating emotional words into sentence context. Event-related potentials (ERPs) to affectively negative, neutral, and positive words, which were either focused or nonfocused in question_–answer pairs, were evaluated during sentence comprehension. The results revealed an early negative effect (90–200 ms), a P2 effect, as well as an effect in the N400 time window, for both emotional salience and information structure. Moreover, an interaction between emotional salience and information structure occurred within the N400 time window over right posterior electrodes, showing that information structure influences the semantic integration only for neutral words, but not for emotional words. This might reflect the fact that the linguistic salience of emotional words can override the effect of information structure on the integration of words into context. The interaction provides evidence for attention–emotion interactions at a later stage of processing. In addition, the absence of interaction in the early time window suggests that the processing of emotional information is highly automatic and independent of context. The results suggest independent attention capture systems of emotional salience and information structure at the early stage but an interaction between them at a later stage, during the semantic integration of words.     

More emotional facial expressions during episodic than during semantic autobiographical retrieval

There is a substantial body of research on the relationship between emotion and autobiographical memory. Using facial analysis software, our study addressed this relationship by investigating basic emotional facial expressions that may be detected during autobiographical recall. Participants were asked to retrieve 3 autobiographical memories, each of which was triggered by one of the following cue words: happy, sad, and city. The autobiographical recall was analyzed by a software for facial analysis that detects and classifies basic emotional expressions. Analyses showed that emotional cues triggered the corresponding basic facial expressions (i.e., happy facial expression for memories cued by happy). Furthermore, we dissociated episodic and semantic retrieval, observing more emotional facial expressions during episodic than during semantic retrieval, regardless of the emotional valence of cues. Our study provides insight into facial expressions that are associated with emotional autobiographical memory. It also highlights an ecological tool to reveal physiological changes that are associated with emotion and memory.     

Affect and retrieval of personal memories

The relationship of pleasantness and intensity of affect to retrieval of reallife experiences was investigated in three experiments. Subjects reported the first specific personal experience that came to mind for a series of prompt words. Latency of report was regarded as a measure of memory accessibility. The first study compared retrieval time for prompts that sampled affects varying in pleasantness and intensity. Experiments II and III assessed the possible contributions of demand characteristics and implicit inferential processes to retrospective judgments of feelings. Judgments of the intensity of feeling engendered when the events occurred were inversely related to report latency. Results support the conclusion that intensity ratings were reliable indices of memory information rather than inferences or reconstructions mediated by report latency. Other characteristics of recollections such as pleasantness, recency, or relative frequency of the specific affects were not correlated with report latency. Two explanations of the findings are considered: an arousal hypothesis and an extent-of-processing hypothesis. The latter provides the most adequate account and relates the present findings to a more general theory of memory processes. The results are also relevant to investigations of mood-dependent retrieval.This is an expanded version of a paper presented in the Symposium on Naturally Occurring Memories, at the meeting of the American Psychological Association, Toronto, August 1978.     

Blurring of emotional and non-emotional memories by taxing working memory during recall

Memories that are recalled while working memory (WM) is taxed, e.g., by making eye movements (EM), become blurred during the recall + EM and later recall, without EM. This may help to explain the effects of Eye Movement and Desensitisation and Reprocessing (EMDR) in the treatment of post-traumatic stress disorder (PTSD) in which patients make EM during trauma recall. Earlier experimental studies on recall + EM have focused on emotional memories. WM theory suggests that recall + EM is superior to recall only but is silent about effects of memory emotionality. Based on the emotion and memory literature, we examined whether recall + EM has superior effects in blurring emotional memories relative to neutral memories. Healthy volunteers recalled negative or neutral memories, matched for vividness, while visually tracking a dot that moved horizontally (“recall + EM”) or remained stationary (“recall only”). Compared to a pre-test, a post-test (without concentrating on the dot) replicated earlier findings: negative memories are rated as less vivid after “recall + EM” but not after “recall only”. This was not found for neutral memories. Emotional memories are more taxing than neutral memories, which may explain the findings. Alternatively, transient arousal induced by recall of aversive memories may promote reconsolidation of the blurred memory image that is provoked by EM.     

Amygdala oscillations and the consolidation of emotional memories

The amygdala receives multi-modal sensory inputs and projects to virtually all levels of the central nervous system. Via these widespread projections, the amygdala facilitates consolidation of emotionally arousing memories. How the amygdala promotes synaptic plasticity elsewhere in the brain remains unknown, however. Recent work indicates that amygdala neurons show theta activity during emotional arousal, and various types of oscillations during sleep. These synchronized neuronal events could promote synaptic plasticity by facilitating interactions between neocortical storage sites and temporal lobe structures involved in declarative memory.     

The emergence of strategic knowledge activation in categorical clustering during retrieval

Elementary school children's free recall clustering has recently been explained as an automatic by-product of their developing knowledge base. In contrast, it is claimed that as children get older they become aware of the usefulness of category organization as a memory strategy that enables them to strategically activate category knowledge even during retrieval. To test this hypothesis an experimental procedure was developed where Ss first had to learn items in a noncategorical order to the criterion of two perfect serial recall trials. After a 12- to 15-min retention interval Ss unexpectedly received either serial or free recall (or--in Experiment 1--cued recall) instructions. In three experiments with second and fourth graders it was shown that (1) fourth graders' recall exceeded that of second graders only in the free, but not in the serial (or cued), recall condition, (2) higher levels of clustering were observed for fourth graders in the free recall condition, and (3) the grade effect on free recall data was eliminated when the influence of metamemory and categorical clustering statistically was partialled out (Experiments 1 and 3). This pattern of results proved robust against variants in which a metamemory question was asked or omitted prior to recall (Experiment 2) and manipulations in which age differences in categorical knowledge were minimized (Experiment 3). The results were interpreted as demonstrating fourth graders' strategic competence in activating category knowledge during retrieval and second graders' automatic knowledge activation.     

Attachment and autobiographical memory retrieval: Event-related potential evidence from strategic information processing

This article presents two studies using event-related potentials combined with an autobiographical memory (AM) retrieval task and a lexical judge task to explore differences in AM retrieval among differently attached individuals and to further explore whether the source of these differences is the schematic information processing mode or strategic information processing mode. The effectiveness of the information processing mode is also studied. The results revealed that differences in the AM extraction of different attachment styles were due to the strategic information processing mode, while no differences were found in the schematic information processing used by individuals with different attachment styles. Further, the strategic information processing used by the securely attached group was more flexible and efficient than that used by the insecurely attached group; moreover, the strategic information processing mode used by the avoidantly attached group was more stable and consistent than that used by the anxiously attached group.     

Electrophysiological indices of emotion processing during retrieval of autobiographical memories by school-age children

We used event-related potentials (ERPs) to examine emotion processing during retrieval of emotional autobiographical memories by school-age children. We initiated processing of the emotional experiences using neutral cue words. On one-third of trials, children were instructed to think of a memory of a negative event, and on another third of trials, they were instructed to think of a memory of a positive event. We then recorded ERPs from 32 electrode sites as the children processed the emotional memories again later in the testing session. The 7- to 10-year-old children generated memories appropriate to the valences specified in the instructions. Neural responses differed as a function of the emotional valence of the events associated with the cues and as a function of gender. In the sample as a whole, differential processing of positive relative to negative and neutral emotions was apparent at posterior electrode sites 1,000–1,500 ms after stimulus onset. For girls, the effect was apparent beginning at 500 ms. No differences between the neural responses to negative and neutral stimuli were observed. At frontal electrode sites, girls evidenced faster processing of positive than of negative emotion, whereas boys evidenced faster processing of negative than of positive emotion. In conclusion, we discuss the possible origins of gender-differential patterns of neural processing.     

Body posture facilitates retrieval of autobiographical memories

We assessed potential facilitation of congruent body posture on access to and retention of autobiographical memories in younger and older adults. Response times were shorter when body positions during prompted retrieval of autobiographical events were similar to the body positions in the original events than when body position was incongruent. Free recall of the autobiographical events two weeks later was also better for congruent-posture than for incongruent-posture memories. The findings were similar for younger and older adults, except for the finding that free recall was more accurate in younger adults than in older adults in the congruent condition. We discuss these findings in the context of theories of embodied cognition.     

Selective memory retrieval can impair and improve retrieval of other memories

Research from the past decades has shown that retrieval of a specific memory (e.g., retrieving part of a previous vacation) typically attenuates retrieval of other memories (e.g., memories for other details of the event), causing retrieval-induced forgetting. More recently, however, it has been shown that retrieval can both attenuate and aid recall of other memories (K.-H. T. B?uml & A. Samenieh, 2010). To identify the circumstances under which retrieval aids recall, the authors examined retrieval dynamics in listwise directed forgetting, context-dependent forgetting, proactive interference, and in the absence of any induced memory impairment. They found beneficial effects of selective retrieval in listwise directed forgetting and context-dependent forgetting but detrimental effects in all the other conditions. Because context-dependent forgetting and listwise directed forgetting arguably reflect impaired context access, the results suggest that memory retrieval aids recall of memories that are subject to impaired context access but attenuates recall in the absence of such circumstances. The findings are consistent with a 2-factor account of memory retrieval and suggest the existence of 2 faces of memory retrieval.     

False memories of emotional and neutral words

This study used the Deese-Roediger-McDermott paradigm to investigate the direction and the extent to which emotional valence in semantic word lists influences the formation of false memories (FM). The experimental paradigm consisted of 1) a study phase (learning of neutral and negative lists of words semantically associated to a non-presented critical lure (CL), 2) a free recall phase, and 3) a recognition phase. Participants had to indicate whether the displayed item was "new" (new item or non-studied CL) or "old" (studied list item). CL associated with negative word lists elicited significantly more FM than CL associated with neutral word lists. This finding is in contrast to previous work showing that emotional words elicit fewer FM than neutral words. The results of our study also suggest that valence is capable of influencing emotional memory in terms of encoding and retrieval processes.     

Event-related potential (ERP) evidence for varied recollection during source monitoring

The source monitoring framework (SMF; M. K. Johnson, S. Hashtroudi, & D. S. Lindsay, 1993) posits that source monitoring can be supported by varying degrees of recollection. Source judgments were made for words heard at study (male or female voice) followed by remember/know (RK) judgments in order to assess differences in degrees of recollection during source monitoring (J. L. Hicks, R. L. Marsh, & L. Ritschel, 2002). The neural correlate of recollection was examined by contrasting event-related potentials (ERPs) for R and K responses that followed accurate source judgments. The recollection ERP effect was greater for R than K responses but greater for K responses than correct rejections, which reinforces the behavioral evidence that indicates source monitoring can be supported by varying degrees of recollection. A robust late posterior negativity ERP effect was present and began earlier for accurate source judgments given subsequent R than K responses. This is interpreted as reflecting systematic decision processes that are described by the SMF.     

The face of memory: experiential avoidance and facial expressions during the retrieval of autobiographical memories

ABSTRACT

Experiential avoidance refers to attempts to control or suppress unwanted thoughts, feelings and emotions. We investigated whether experiential avoidance is associated with fewer facial expressions during autobiographical retrieval (i.e. retrieval of memory for personal information). We invited participants to retrieve autobiographical memories, and recall was analysed by a facial analysis software that detects and classifies emotional expressions. Participants were divided into high vs. low experiential avoidance. Analysis showed fewer emotional facial expressions in participants with high experiential avoidance than in those with low experiential avoidance during autobiographical retrieval. This low emotional expression can be regarded as an attempt by individuals with high experiential avoidance to avoid communicating the emotional load to others. This low emotional expression can be also regarded as an attempt by individuals with high experiential avoidance to control or suppress the internal events that contribute to the appearance or persistence of unwanted emotional states during retrieval.     

False memories in obstructive sleep apnoea syndrome: evidence from the divided attention paradigm at encoding or retrieval

ABSTRACT

Patients with obstructive sleep apnoea syndrome (OSAS) exhibit impaired retrieval of item-specific information, increasing their propensity to generate false recognitions. The present study investigated the effect of OSAS on false recognition, using a divided-attention paradigm to examine whether reducing the availability of attentional resources during encoding or retrieval in healthy participants mimics the effect of OSAS. We tested four groups of participants, using the Deese – Roediger – McDermott paradigm: patients with OSAS and controls, either under full attention or under divided attention at encoding or retrieval. Results showed that divided attention at retrieval, but not at encoding, mimicked the effects of OSAS on memory performance, as controls in this group exhibited a higher level of false recognition than those under full attention, but a similar level of correct recognition. Our results suggest that the greater susceptibility of patients with OSAS to false recognition may be due to a limited availability of attentional resources, which may specifically disrupt retrieval processes.