The effects of valence and arousal on the neural activity leading to subsequent memory

This study examined how valence and arousal affect the processes linked to subsequent memory for emotional information. While undergoing an fMRI scan, participants viewed neutral pictures and emotional pictures varying by valence and arousal. After the scan, participants performed a recognition test. Subsequent memory for negative or high arousal information was associated with occipital and temporal activity, whereas memory for positive or low arousal information was associated with frontal activity. Regression analyses confirmed that for negative or high arousal items, temporal lobe activity was the strongest predictor of later memory whereas for positive or low arousal items, frontal activity corresponded most strongly with later memory. These results suggest that the types of encoding processes relating to memory (e.g., sensory vs. elaborative processing) can differ based on the affective qualities of emotional information.     

The effect of age on memory for emotional faces

Prior studies of emotion suggest that young adults should have enhanced memory for negative faces and that this enhancement should be reduced in older adults. Several studies have not shown these effects but were conducted with procedures different from those used with other emotional stimuli. In this study, researchers examined age differences in recognition of faces with emotional or neutral expressions, using trial-unique stimuli, as is typically done with other types of emotional stimuli. They also assessed the influence of personality traits and mood on memory. Enhanced recognition for negative faces was found in young adults but not in older adults. Recognition of faces was not influenced by mood or personality traits in young adults, but lower levels of extraversion and better emotional sensitivity predicted better negative face memory in older adults. These results suggest that negative expressions enhance memory for faces in young adults, as negative valence enhances memory for words and scenes. This enhancement is absent in older adults, but memory for emotional faces is modulated in older adults by personality traits that are relevant to emotional processing.     

Age differences in perception and awareness of emotion

We investigated the effects of age and gender on emotional perception and physiology using electrodermal skin conductance response (SCR) and examined whether SCR is related to subjective perceptions of emotional pictures. Older adults found pictures to be more positive and arousing than younger participants. Older women rated pictures more extremely at both ends of the valence continuum: they rated positive pictures more positively and negative pictures more negatively. Elders were less likely to show measurable SCRs. However, magnitude of SCRs when a response occurred did not differ between young and old. Subjective ratings of emotion correlated with physiological responses in younger participants, but they were unrelated in older participants. Thus, in older adults the perception of emotional events was disconnected from the physiological state induced by emotion.     

Neural processing of emotional pictures and words: a comparison of young and older adults

Recent findings have revealed age-related changes in neural recruitment during the processing of emotional information. The present study examined whether these age-related changes would be more pronounced for words, thought to be processed in a controlled manner versus relatively automatically processed pictures. Compared to young adults, older adults showed less amygdala activation, and more medial prefrontal cortex (PFC) activation, for negative than positive pictures. The opposite pattern was observed for words. Older adults showed a positivity effect in memory for words, but not for pictures, suggesting that their positivity effect may stem from age-related changes in medial PFC engagement during encoding.     

The neural fate of neutral information in emotion‐enhanced memory

In this study, we report evidence that neural activity reflecting the encoding of emotionally neutral information in memory is reduced when neutral and emotional stimuli are intermixed during encoding. Specifically, participants studied emotional and neutral pictures organized in mixed lists (in which emotional and neutral pictures were intermixed) or in pure lists (only‐neutral or only‐emotional pictures) and performed a recall test. To estimate encoding efficiency, we used the Dm effect, measured with event‐related potentials. Recall for neutral items was lower in mixed compared to pure lists and posterior Dm activity for neutral items was reduced in mixed lists, whereas it remained robust in pure lists. These findings might be caused by an asymmetrical competition for attentional and working memory resources between emotional and neutral information, which could be a major determinant of emotional memory effects.     

Behavioural and electrophysiological effects of visual paired associate context manipulations during encoding and recognition in younger adults,older adults and older cognitively declined adults

The current study examined the EEG of young, old and old declined adults performing a visual paired associate task. In order to examine the effects of encoding context and stimulus repetition, target pairs were presented on either detailed or white backgrounds and were repeatedly presented during both early and late phases of encoding. Results indicated an increase in P300 amplitude in the right parietal cortex from early to late stages of encoding in older declined adults, whereas both younger adults and older controls showed a reduction in P300 amplitude in this same area from early to late phase encoding. In the right hemisphere, stimuli encoded with a white background had larger P300 amplitudes than stimuli presented with a detailed background; however, in the left hemisphere, in the later stages of encoding, stimuli presented with a detailed background had larger amplitudes than stimuli presented with a white background. Behaviourally, there was better memory for congruent stimuli reinstated with a detailed background, but this finding was for older controls only. During recognition, there was a general trend for congruent stimuli to elicit a larger amplitude response than incongruent stimuli, suggesting a distinct effect of context reinstatement on underlying patterns of physiological responding. However, behavioural data suggest that older declined adults showed no memory benefits associated with context reinstatement. When compared with older declined adults, younger adults had larger P100 amplitude responses to stimuli presented during recognition, and overall, younger adults had faster recognition reaction times than older control and older declined adults. Further analysis of repetition effects and context-based hemispheric asymmetry may prove informative in identifying declining memory performance in the elderly, potentially before it becomes manifested behaviourally.     

Event‐related potentials of emotional and neutral memories: The role of encoding position and delayed testing

Previous research found that memory is not only better for emotional information but also for neutral information that has been encoded in the context of an emotional event. In the present ERP study, we investigated two factors that may influence memory for neutral and emotional items: temporal proximity between emotional and neutral items during encoding, and retention interval (immediate vs. delayed). Forty‐nine female participants incidentally encoded 36 unpleasant and 108 neutral pictures (36 neutral pictures preceded an unpleasant picture, 36 followed an unpleasant picture, and 36 neutral pictures were preceded and followed by neutral pictures) and participated in a recognition memory task either immediately (N = 24) or 1 week (N = 25) after encoding. Results showed better memory for emotional pictures relative to neutral pictures. In accordance, enhanced centroparietal old/new differences (500–900 ms) during recognition were observed for unpleasant compared to neutral pictures, most pronounced for the 1‐week interval. Picture position effects, however, were only subtle. During encoding, late positive potentials for neutral pictures were slightly lower for neutral pictures following unpleasant ones, but only at trend level. To summarize, we could replicate and extend previous ERP findings showing that emotionally arousing events are better recollected than neutral events, particularly when memory is tested after longer retention intervals. Picture position during encoding, however, had only small effects on elaborative processing and no effects on memory retrieval.     

Dopamine and frontostriatal networks in cognitive aging

Recent studies have linked dopamine to differences in behavior and brain activity in normal individuals. We explored these relationships in older and younger adults by investigating how functional connectivity between the striatum and prefrontal cortex is related to caudate dopamine and verbal working memory task performance. We studied 12 young and 18 older participants with functional magnetic resonance imaging (fMRI) during this task, and used positron emission tomography with the tracer 6-[¹⁸F]-fluoro-L-m-tyrosine (FMT) to assess dopamine synthesis capacity. Younger adults had a greater extent of frontal caudate functional connectivity during the load-dependent delay period of the working memory task than the older participants. Across all subjects, the extent of this functional connectivity was negatively correlated with dopamine synthesis capacity, such that participants with the greatest connectivity had the lowest caudate 6-[¹⁸F]-fluoro-L-m-tyrosine (FMT) signal. Additionally, the extent of functional connectivity was positively correlated with working memory performance. Overall these data suggest interdependencies exist between frontostriatal functional connectivity, dopamine, and working memory performance and that this system is functioning suboptimally in normal aging.     

Sleep deprivation impairs binding of information with its context

Binding information to its context in long-term memory is critical for many tasks, including memory tasks and decision making. Failure to associate information to its context could be an important aspect of sleep deprivation effects on cognition, but little is known about binding problems from being sleep-deprived at the time of encoding. We studied how sleep deprivation affects binding using a well-established paradigm testing the ability to remember auditorily presented words (items) and their speakers (source context). In a laboratory study, 68 healthy young adults were randomly assigned to total sleep deprivation or a well-rested control condition. Participants completed an affective item and source memory task twice: once after 7-hour awake during baseline and again 24 hours later, after nearly 31 hours awake in the total sleep deprivation condition or 7 hours awake in the control condition. Participants listened to negative, positive, and neutral words presented by a male or female speaker and were immediately tested for recognition of the words and their respective speakers. Recognition of items declined during sleep deprivation, but even when items were recognized accurately, recognition of their associated sources also declined. Negative items were less bound with their sources than positive or neutral items, but sleep deprivation did not significantly affect this pattern. Our findings indicate that learning while sleep-deprived disrupts the binding of information to its context independent of item valence. Such binding failures may contribute to sleep deprivation effects on tasks requiring the ability to bind new information together in memory.     

Retrospective attention enhances visual working memory in the young but not the old: An ERP study

Behavioral evidence from the young suggests spatial cues that orient attention toward task‐relevant items in visual working memory (VWM) enhance memory capacity. Whether older adults can also use retrospective cues (“retro‐cues”) to enhance VWM capacity is unknown. In the current event‐related potential (ERP) study, young and old adults performed a VWM task in which spatially informative retro‐cues were presented during maintenance. Young but not older adults' VWM capacity benefited from retro‐cueing. The contralateral delay activity (CDA) ERP index of VWM maintenance was attenuated after the retro‐cue, which effectively reduced the impact of memory load. CDA amplitudes were reduced prior to retro‐cue onset in the old only. Despite a preserved ability to delete items from VWM, older adults may be less able to use retrospective attention to enhance memory capacity when expectancy of impending spatial cues disrupts effective VWM maintenance.     

Changes in whole-brain functional networks and memory performance in aging

We used resting-functional magnetic resonance imaging data from 98 healthy older adults to analyze how local and global measures of functional brain connectivity are affected by age, and whether they are related to differences in memory performance. Whole-brain networks were created individually by parcellating the brain into 90 cerebral regions and obtaining pairwise connectivity. First, we studied age-associations in interregional connectivity and their relationship with the length of the connections. Aging was associated with less connectivity in the long-range connections of fronto-parietal and fronto-occipital systems and with higher connectivity of the short-range connections within frontal, parietal, and occipital lobes. We also used the graph theory to measure functional integration and segregation. The pattern of the overall age-related correlations presented positive correlations of average minimum path length (r = 0.380, p = 0.008) and of global clustering coefficients (r = 0.454, p < 0.001), leading to less integrated and more segregated global networks. Main correlations in clustering coefficients were located in the frontal and parietal lobes. Higher clustering coefficients of some areas were related to lower performance in verbal and visual memory functions. In conclusion, we found that older participants showed lower connectivity of long-range connections together with higher functional segregation of these same connections, which appeared to indicate a more local clustering of information processing. Higher local clustering in older participants was negatively related to memory performance.     

Age differences in the emotional modulation of ERP old/new effects

The emotional salience of stimuli influences ERP old/new effects, but despite proven age differences in emotional processing, the influence of emotion on old/new effects has previously been investigated in younger adults only. Therefore, we set out to examine age differences in the emotional modulation of old/new effects. To this end, the electroencephalogram of younger (17-27 years) and older (63-77 years) adults was recorded while they completed a continuous recognition test with unpleasant, neutral and pleasant pictures. Because recollection is typically enhanced by emotion, the parietal old/new effect was expected to be larger for emotional than neutral stimuli in the younger adults. Because recollection suffers from age-related decline, emotion enhancement of the parietal old/new effect was not expected in the older adults. The results showed that, in both age groups, recognition accuracy was not affected by emotion and that the response bias was more liberal for unpleasant pictures. The younger adults displayed an early, a parietal and a late frontal old/new effect, whereas the older adults showed an early, no parietal and an inverse left-lateralized late frontal old/new effect. Further, the emotional modulation of the old/new effects differed with age. Importantly, emotion enhanced the parietal and late frontal old/new effects in younger adults, and the early old/new effect in older adults. This suggests that whereas recollection and post-retrieval processes are augmented in emotional recognition memory in younger adults, familiarity is enhanced by emotional salience in older adults.     

Increased alpha suppression with age during involuntary memory retrieval

Recent work suggests that while voluntary episodic memory declines with age, involuntary episodic memory, which comes to mind spontaneously without intention, remains relatively intact. However, the neurophysiology underlying these differences has yet to be established. The current study used electroencephalography (EEG) to investigate voluntary and involuntary retrieval in older and younger adults. Participants first encoded sounds, half of which were paired with pictures, the other half unpaired. EEG was then recorded as they listened to the sounds, with participants in the involuntary group performing a sound localization cover task, and those in the voluntary group additionally attempting to recall the associated pictures. Participants later reported which sounds brought the paired picture to mind during the localization task. Reaction times on the localization task were slower for voluntary than involuntary retrieval and for paired than unpaired sounds, possibly reflecting increased attentional demands of voluntary retrieval and interference from reactivation of the associated pictures respectively. For the EEG analyses, young adults showed greater alpha event-related desynchronization (ERD) during voluntary than involuntary retrieval at frontal and occipital sites, while older adults showed pronounced alpha ERD regardless of intention. Additionally, older adults showed greater ERD for paired than unpaired sounds at occipital sites, likely reflecting visual reactivation of the associated pictures. Young adults did not show this alpha ERD memory effect. Taken together, these data suggest that involuntary memory is largely preserved with age, but this may be due to older adults' greater recruitment of top-down control even when demand for such control is limited.     

Aging increases the susceptibility to motor memory interference and reduces off-line gains in motor skill learning

Declines in the ability to learn motor skills in older adults are commonly attributed to deficits in the encoding of sensorimotor information during motor practice. We investigated whether aging also impairs motor memory consolidation by assessing the susceptibility to memory interference and off-line gains in motor skill learning after practice in children, young, and older adults. Subjects performed a ballistic task (A) followed by an accuracy-tracking task (B) designed to disrupt the consolidation of A. Retention tests of A were performed immediately and 24 hours after B. Older adults showed greater susceptibility to memory interference and no off-line gains in motor skill learning. Performing B produced memory interference and reduced off-line gains only in the older group. However, older adults also showed deficits in memory consolidation independent of the interfering effects of B. Age-related declines in motor skill learning are not produced exclusively by deficits in the encoding of sensorimotor information during practice. Aging also increases the susceptibility to memory interference and reduces off-line gains in motor skill learning after practice.     

Memory load and the cognitive pupillary response in aging

The effect of memory load on the cognitive pupillary response among 16 young adults and 16 older adults was investigated. Mean pupil dilation and reaction time were measured during a Sternberg memory-search task, which involved six levels of memory load. A classic interaction pattern was obtained in which the reaction times of the elderly participants increased more as a function of memory load than the reaction times of the young participants. In the encoding phase of the experiment, mean dilation increased with memory load. No age differences were observed here. In the search phase of the experiment, however, mean pupil dilation was considerably greater in the young than in the elderly participants. Moreover, mean dilation of the older participants was not sensitive to memory load, whereas mean dilation increased as a function of memory load in the young participants. The results suggest that the usefulness of the pupillary response as a correlate of subtle fluctuations in memory load diminishes with old age.     

Neural correlates of source memory retrieval in young, middle-aged and elderly adults

Event-related potentials (ERPs) were recorded in young (21-27 years old), middle-aged (50-57 years old) and older adults (70-77 years old) to determine whether the decline in source memory that occurs with advancing age coincides with contemporaneous neurophysiological changes. Source memory for the spatial location (quadrant on the screen) of images presented during encoding was examined. The images were shown in the center of the screen during the retrieval task. Retrieval success for source information was characterized by different scalp topographies at frontal electrode sites in young adults relative to middle-aged and older adults. The right frontal effect during unsuccessful retrieval attempts showed amplitude and latency differences across age groups and was related to the ability to discriminate between old and new images only in young adults. These results suggest that the neural correlates of the retrieval success and attempt were affected by age and these effects were present by middle-age.     

Age differences on ERP old/new effects for emotional and neutral faces

This study used event-related potentials (ERPs) to examine age differences in recognition memory for negative and neutral faces that systematically varied in facial expression during encoding and retrieval. During study, younger and older participants viewed negative and neutral faces and were asked to classify each facial expression. During test, half of the facial identities changed their facial expression, while the other half showed the same facial expression. Participants were asked to give old/new judgments to the depicted person. Four main findings were observed. First, when facial emotion did not switch from study to test, negative and neutral faces evoked spatially dissociable ERP old/new effects, independent of age. This suggests that different retrieval mechanisms contributed to successful recognition of negative and neutral faces in both age groups. Second, faces encoded with a negative expression evoked an early occipital old/new effect only in the young, perhaps suggesting superior memory for visual information. Third, faces retrieved with a negative expression evoked in both age groups an early parietal old/new effect, suggesting that negative emotion during retrieval facilitated memory access. Hence, in the early time latency in young adults both encoding-related and retrieval-related emotion effects contributed to face recognition memory, whereas in older adults encoding-related emotion effects were reduced and retrieval-related emotion effects were preserved. Finally, in the late time latency perceptual similarity between study and test faces modified or overruled encoding-related emotion effects in the young and retrieval-related emotion effects in both age groups, respectively.     

An ERP investigation of item-scene incongruity at encoding on subsequent recognition

The aim of the present study was to investigate how item-scene incongruity at encoding influences subsequent item recognition and the associated event-related potential (ERP) old/new effects. Participants (N = 26) studied pictures showing an item in a scene, either in a congruent condition (e.g., a tent in a field) or an incongruent condition (e.g., a shower cabin in a field). Items were presented alone at test. Behavioral data revealed a benefit of incongruent information, with greater source memory performance but no significant effect on old/new recognition judgments. Longer response times for old compared to new items showed that participants not only evaluated the old-new status of objects during recognition, but also worked already on the scene context decision relative to the source memory judgment. An ERP incongruity effect was found at study, with greater N400 amplitude in the incongruent condition than the congruent condition. During recognition, the results provide evidence that item-scene incongruity at study increases the amplitude of ERP old/new effects. A mid-frontal N400 old/new effect was found in the early time window (300–500 ms), and a right frontal sub-component was modulated by item-scene incongruity at encoding. The modulation observed in the later time window (500–800 ms) confirmed previous studies showing that the parietal old/new effect reflects the retrieval of episodic contextual details. The present study shows that the magnitude of ERP old/new effects is sensitive to item-scene incongruity at encoding from the early time window in the right frontal region to the later retrieval processes.     

Effects of aging on functional connectivity of the amygdala during negative evaluation: a network analysis of fMRI data

Previous evidence has suggested both preserved emotional function in aging and age-related differences in emotional processing, but the neural networks underlying such processing alterations in the context of preserved affective function are not clear. Using event-related fMRI, we scanned young and older adults while they made valence ratings for emotional pictures. Behavioral results showed a similar pattern of emotional evaluation, but older adults experienced negatively valenced pictures as being less negative. Consistent with behavioral findings, we identified common activity in the right amygdala, but age-related differences in the functional connectivity of this region with the rest of the brain. Compared to young adults, older adults had greater functional connectivity between the right amygdala and ventral anterior cingulate cortex, possibly reflecting increased emotional regulation. Conversely, older adults showed decreased functional connectivity with posterior brain regions, likely reflecting decreased perceptual processing. Thus, age-related differences in evaluating negatively valenced stimuli might reflect decreased perceptual processing of these stimuli, as well as the engagement of control processes that inhibit the response to negative emotion.     

Neural recruitment and connectivity during emotional memory retrieval across the adult life span

Although research has identified age-related changes in neural recruitment during emotional memory encoding, it is unclear whether these differences extend to retrieval. In this study, participants engaged in a recognition task during a functional magnetic resonance imaging scan. They viewed neutral titles and indicated whether each title had been presented with an image during the study phase. Neural activity and connectivity during retrieval of titles associated with positive and negative images were compared with age (treated as a continuous variable) included as a regressor of interest. Aging was associated with increased prefrontal activation for retrieval of positive and negative memories, but this pattern was more widespread for negative memories. Aging also was associated with greater negative connectivity between a left hippocampal seed region and multiple regions of prefrontal cortex, but this effect of age occurred during negative retrieval only. These findings demonstrate that age-related changes in prefrontal recruitment and connectivity during retrieval depend on memory valence. The use of a life span approach also emphasized both continuities and discontinuities in recruitment and connectivity across the adult life span, highlighting the insights to be gained from using a full life span sample.