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Recent evidence points to enhanced episodic memory retrieval not only for emotional items but also for neutral information encoded in emotional contexts. However, prior research only tested instructed explicit recognition, and hence here we investigated whether memory retrieval is also heightened for cues from emotional contexts when retrieval is not explicitly probed. During the first session of a two-session experiment, neutral objects were presented on different background scenes varying in emotional and neutral contents. One week later, objects were presented again (with no background) intermixed with novel objects. In both sessions, participants were instructed to attentively watch the stimuli (free viewing procedure), and during the second session, ERPs were also collected to measure the ERP Old/New effect, an electrophysiological correlate of episodic memory retrieval. Analyses were performed using cluster-based permutation tests in order to identify reliable spatiotemporal ERP differences. Based on this approach, old relative to new objects, were associated with larger ERP positivity in an early (364-744 ms) and late time window (760-1148 ms) over distinct central electrode clusters. Interestingly, significant late ERP Old/New differences were only observed for objects previously encoded with emotional, but not neutral scenes (504 to 1144 ms). Because these ERP differences were observed in a non-instructed retrieval context, our results indicate that long-term, spontaneous retrieval for neutral objects, is particularly heightened if encoded within emotionally salient contextual information. These findings may assist in understanding mechanisms underlying spontaneous retrieval of emotional associates and the utility of ERPs to study maladaptive involuntary memories in trauma- and stress-related disorders.
Recent research indicates that non- invasive stimulation of the afferent auricular vagal nerve (tVNS) may modulate various cognitive and affec-tive functions, likely via activation of the locus coeruleus- norepinephrine (LC- NE) system. In a series of ERP studies we found that the attention- related P300 component is enhanced during continuous vagal stimula-tion, compared to sham, which is also related to increased salivary alpha amylase levels (a putative indirect marker for central NE activation). In another study, we investigated the effect of continuous tVNS on the late positive potential (LPP), an electrophysiological index for motivated atten-tion toward emotionally evocative cues, and the effects of tVNS on later recognition memory (1- week delay). Here, vagal stimulation prompted earlier LPP differences (300- 500 ms) between unpleasant and neutral scenes. During retrieval, vagal stimulation significantly improved memory performance for unpleasant, but not neutral pictures, compared to sham stimulation, which was also related to enhanced salivary alpha amylase levels. In line, unpleasant images encoded under tVNS compared to sham stimulation also produced enhanced ERP old/new differences (500- 800 ms) during retrieval indicating better recollection. Taken together, our studies suggest that tVNS facilitates attention, learning and episodic memory, likely via afferent projections to the arousal- modulated LC- NE system. We will, however, also show data that point to critical stimulation parameters (likely duration and frequency) that need to be considered when applying tVNS
Chronic stress and emotion: Differential effects on attentional processing and recognition memory
(2019)
Previous research indicates that acute stress around the time of learning facilitates attention and memory for emotionally salient information. Despite accumulating evidence for these acute stress effects, less is known about the role of chronic stress. In the present study, we therefore tested emotional and neutral scene processing and later recognition memory in female participants using hair cortisol concentrations as a biological marker for chronic stress. Event-related potentials recorded during picture viewing indicated enhanced late positive potentials (LPPs) for emotional, relative to neutral contents. These brain potentials varied as a function of long-term hair cortisol levels: hair-cortisol levels were positively related to overall LPP amplitudes. Results from recognition memory testing one week after encoding revealed better memory for emotional relative to neutral scenes. Hair-cortisol levels, however, were related to poorer memory accuracy. Taken together, our results indicate that chronic stress enhanced attentional processing during encoding of new stimuli and impaired later recognition memory. Results are discussed with regard to putatively opposite effects of chronic stress on certain brain regions (e.g., amygdala and hippocampus).
Despite the widespread use of oral contraceptives (OCs), remarkably little is known about the effects of OCs on emotion, cognition, and behavior. However, coincidental findings suggest that OCs impair the ability to recognize others’ emotional expressions, which may have serious consequences in interpersonal contexts. To further investigate the effects of OCs on emotion recognition, we tested whether women who were using OCs (n = 42) would be less accurate in the recognition of complex emotional expressions than women who were not using OCs (n = 53). In addition, we explored whether these differences in emotion recognition would depend on women’s menstrual cycle phase. We found that women with OC use were indeed less accurate in the recognition of complex expressions than women without OC use, in particular during the processing of expressions that were difficult to recognize. These differences in emotion recognition did not depend on women’s menstrual cycle phase. Our findings, thus, suggest that OCs impair women’s emotion recognition, which should be taken into account when informing women about the side-effects of OC use.
Due to their ability to capture attention, emotional stimuli tend to benefit from enhanced perceptual processing, which can be helpful when such stimuli are task-relevant but hindering when they are task-irrelevant. Altered emotion-attention interactions have been associated with symptoms of affective disturbances, and emerging research focuses on improving emotion-attention interactions to prevent or treat affective disorders. In line with the Human Affectome Project's emphasis on linguistic components, we also analyzed the language used to describe attention-related aspects of emotion, and highlighted terms related to domains such as conscious awareness, motivational effects of attention, social attention, and emotion regulation. These terms were discussed within a broader review of available evidence regarding the neural correlates of (1) Emotion-Attention Interactions in Perception, (2) Emotion-Attention Interactions in Learning and Memory, (3) Individual Differences in Emotion-Attention Interactions, and (4) Training and Interventions to Optimize Emotion-Attention Interactions. This comprehensive approach enabled an integrative overview of the current knowledge regarding the mechanisms of emotion-attention interactions at multiple levels of analysis, and identification of emerging directions for future investigations.
Due to their ability to capture attention, emotional stimuli tend to benefit from enhanced perceptual processing, which can be helpful when such stimuli are task-relevant but hindering when they are task-irrelevant. Altered emotion-attention interactions have been associated with symptoms of affective disturbances, and emerging research focuses on improving emotion-attention interactions to prevent or treat affective disorders. In line with the Human Affectome Project's emphasis on linguistic components, we also analyzed the language used to describe attention-related aspects of emotion, and highlighted terms related to domains such as conscious awareness, motivational effects of attention, social attention, and emotion regulation. These terms were discussed within a broader review of available evidence regarding the neural correlates of (1) Emotion-Attention Interactions in Perception, (2) Emotion-Attention Interactions in Learning and Memory, (3) Individual Differences in Emotion-Attention Interactions, and (4) Training and Interventions to Optimize Emotion-Attention Interactions. This comprehensive approach enabled an integrative overview of the current knowledge regarding the mechanisms of emotion-attention interactions at multiple levels of analysis, and identification of emerging directions for future investigations.
Influence of resting heart rate variability on affect processing in different induction contexts
(2020)
Procrastination is a self-regulatory problem of voluntarily and destructively delaying intended and necessary or personally important tasks. Previous studies showed that procrastination is associated with executive dysfunctions that seem to be particularly strong in punishing contexts. In the present event-related potential (ERP) study a monetary version of the parametric Go/No-Go task was performed by high and low academic procrastinators to verify the influence of motivational context (reward vs. punishment expectation) and task difficulty (easy vs. hard) on procrastination-related executive dysfunctions. The results revealed increased post-error slowing along with reduced P300 and error-related negativity (ERN) amplitudes in high (vs. low) procrastination participants-effects that indicate impaired attention and error-related processing in this group. This pattern of results did not differ as a function of task difficulty and motivation condition. However, when the task got more difficult executive attention deficits became even more apparent at the behavioral level in high procrastinators, as indexed by increased reaction time variability. The findings substantiate prior preliminary evidence that procrastinators show difficulties in certain aspects of executive functioning (in attention and error processing) during execution of task-relevant behavior, which may be more apparent in highly demanding situations.
In his seminal works, Endel Tulving argued that functionally distinct memory systems give rise to subjective experiences of remembering and knowing (i.e., recollection- vs. familiarity-based memory, respectively). Evidence shows that emotion specifically enhances recollection, and this effect is subserved by a synergistic mechanism involving the amygdala (AMY) and hippocampus (HC). In extreme circumstances, however, uncontrolled recollection of highly distressing memories may lead to symptoms of affective disorders. Therefore, it is important to understand the factors that can diminish such detrimental effects. Here, we investigated the effects of Focused Attention (FA) on emotional recollection. FA is an emotion regulation strategy that has been proven quite effective in reducing the impact of emotional responses associated with the recollection of distressing autobiographical memories, but its impact during emotional memory encoding is not known. Functional MRI and eye-tracking data were recorded while participants viewed a series of composite negative and neutral images with distinguishable foreground (FG) and background (BG) areas. Participants were instructed to focus either on the FG or BG content of the images and to rate their emotional responses. About 4 days later, participants' memory was assessed using the R/K procedure, to indicate whether they Recollected specific contextual details about the encoded images or the images were just familiar to them - i.e., participants only Knew that they saw the pictures without being able to remember specific contextual details. First, results revealed that FA was successful in decreasing memory for emotional pictures viewed in BG Focus condition, and this effect was driven by recollection-based retrieval. Second, the BG Focus condition was associated with decreased activity in the AMY, HC, and anterior parahippocampal gyrus for subsequently recollected emotional items. Moreover, correlation analyses also showed that reduced activity in these regions predicted greater reduction in emotional recollection following FA. These results demonstrate the effectiveness of FA in mitigating emotional experiences and emotional recollection associated with unpleasant emotional events.
Understanding the association between autonomic nervous system [ANS] function and brain morphology across the lifespan provides important insights into neurovisceral mechanisms underlying health and disease. Resting-state ANS activity, indexed by measures of heart rate [HR] and its variability [HRV] has been associated with brain morphology, particularly cortical thickness [CT]. While findings have been mixed regarding the anatomical distribution and direction of the associations, these inconsistencies may be due to sex and age differences in HR/HRV and CT. Previous studies have been limited by small sample sizes, which impede the assessment of sex differences and aging effects on the association between ANS function and CT. To overcome these limitations, 20 groups worldwide contributed data collected under similar protocols of CT assessment and HR/HRV recording to be pooled in a mega-analysis (N = 1,218 (50.5% female), mean age 36.7 years (range: 12-87)). Findings suggest a decline in HRV as well as CT with increasing age. CT, particularly in the orbitofrontal cortex, explained additional variance in HRV, beyond the effects of aging. This pattern of results may suggest that the decline in HRV with increasing age is related to a decline in orbitofrontal CT. These effects were independent of sex and specific to HRV; with no significant association between CT and HR. Greater CT across the adult lifespan may be vital for the maintenance of healthy cardiac regulation via the ANS-or greater cardiac vagal activity as indirectly reflected in HRV may slow brain atrophy. Findings reveal an important association between CT and cardiac parasympathetic activity with implications for healthy aging and longevity that should be studied further in longitudinal research.
Inhibiting fear-related thoughts and defensive behaviors when they are no longer appropriate to the situation is a prerequisite for flexible and adaptive responding to changing environments. Such inhibition of defensive systems is mediated by ventromedial prefrontal cortex (vmPFC), limbic basolateral amygdala (BLA), and brain stem locus-coeruleus noradrenergic system (LC-NAs). Non-invasive, transcutaneous vagus nerve stimulation (tVNS) has shown to activate this circuit. Using a multiple-day single-cue fear conditioning and extinction paradigm, we investigated long-term effects of tVNS on inhibition of low-level amygdala modulated fear potentiated startle and cognitive risk assessments. We found that administration of tVNS during extinction training facilitated inhibition of fear potentiated startle responses and cognitive risk assessments, resulting in facilitated formation, consolidation and long-term recall of extinction memory, and prevention of the return of fear. These findings might indicate new ways to increase the efficacy of exposure-based treatments of anxiety disorders.
Stressful events affect mnemonic processing, in particular for emotionally arousing events. Previous research on the mechanisms underlying stress effects on human memory focused on stress-induced changes in the neural activity elicited by a stimulus. We tested an alternative mechanism and hypothesized that stress may already alter the neural context for successful memory formation, reflected in the neural activity preceding a stimulus. Therefore, 69 participants underwent a stress or control procedure before encoding neutral and negative pictures. During encoding, we recorded high-density EEG and analyzed-based on multivariate searchlight analyses-oscillatory activity and cross-frequency coupling patterns before stimulus onset that were predictive of memory tested 24 hr later. Prestimulus theta predicted subsequent memory in controls but not in stressed participants. Instead, prestimulus gamma predicted successful memory formation after stress, specifically for emotional material. Likewise, stress altered the patterns of prestimulus theta-beta and theta-gamma phase-amplitude coupling predictive of subsequent memory, again depending on the emotionality of the presented material. Our data suggest that stress changes the neural context for building new memories, tuning this neural context specifically to the encoding of emotionally salient events. These findings point to a yet unknown mechanism through which stressful events may change (emotional) memory formation.
Previous clinical research found that invasive vagus nerve stimulation (VNS) enhanced word recognition memory in epileptic patients, an effect assumed to be related to the activation of brainstem arousal systems. In this study, we applied non-invasive transcutaneous auricular VNS (tVNS) to replicate and extend the previous work. Using a single-blind, randomized, between-subject design, 60 healthy volunteers received active or sham stimulation during a lexical decision task, in which emotional and neutral stimuli were classified as words or non-words. In a subsequent recognition memory task (1 day after stimulation), participants' memory performance on these words and their subjective memory confidence were tested. Salivary alpha-amylase (sAA) levels, a putative indirect measure of central noradrenergic activation, were also measured before and after stimulation. During encoding, pleasant words were more accurately detected than neutral and unpleasant words. However, no tVNS effects were observed on task performance or on overall sAA level changes. tVNS also did not modulate overall recognition memory, which was particularly enhanced for pleasant emotional words. However, when hit rates were split based on confidence ratings reflecting familiarity- and recollection-based memory, higher recollection-based memory performance (irrespective of emotional category) was observed during active stimulation than during sham stimulation. To summarize, we replicated prior findings of enhanced processing and memory for emotional (pleasant) words. Whereas tVNS showed no effects on word processing, subtle effects on recollection-based memory performance emerged, which may indicate that tVNS facilitates hippocampus-mediated consolidation processes.
Previous clinical research found that invasive vagus nerve stimulation (VNS) enhanced word recognition memory in epileptic patients, an effect assumed to be related to the activation of brainstem arousal systems. In this study, we applied non-invasive transcutaneous auricular VNS (tVNS) to replicate and extend the previous work. Using a single-blind, randomized, between-subject design, 60 healthy volunteers received active or sham stimulation during a lexical decision task, in which emotional and neutral stimuli were classified as words or non-words. In a subsequent recognition memory task (1 day after stimulation), participants' memory performance on these words and their subjective memory confidence were tested. Salivary alpha-amylase (sAA) levels, a putative indirect measure of central noradrenergic activation, were also measured before and after stimulation. During encoding, pleasant words were more accurately detected than neutral and unpleasant words. However, no tVNS effects were observed on task performance or on overall sAA level changes. tVNS also did not modulate overall recognition memory, which was particularly enhanced for pleasant emotional words. However, when hit rates were split based on confidence ratings reflecting familiarity- and recollection-based memory, higher recollection-based memory performance (irrespective of emotional category) was observed during active stimulation than during sham stimulation. To summarize, we replicated prior findings of enhanced processing and memory for emotional (pleasant) words. Whereas tVNS showed no effects on word processing, subtle effects on recollection-based memory performance emerged, which may indicate that tVNS facilitates hippocampus-mediated consolidation processes.
Emotional memories are better remembered than neutral ones, but the mechanisms leading to this memory bias are not well under-stood in humans yet. Based on animal research, it is suggested that the memory-enhancing effect of emotion is based on central nor-adrenergic release, which is triggered by afferent vagal nerve activation. To test the causal link between vagus nerve activation and emotional memory in humans, we applied continuous noninvasive transcutaneous auricular vagus nerve stimulation (taVNS) during exposure to emotional arousing and neutral scenes and tested subsequent, long-term recognition memory after 1 week. We found that taVNS, compared with sham, increased recollection-based memory performance for emotional, but not neutral, material. These findings were complemented by larger recollection-related brain potentials (parietal ERP Old/New effect) during retrieval of emotional scenes encoded under taVNS, compared with sham. Furthermore, brain potentials recorded during encoding also revealed that taVNS facilitated early attentional discrimination between emotional and neutral scenes. Extending animal research, our behavioral and neu-ral findings confirm a modulatory influence of the vagus nerve in emotional memory formation in humans.
The Role of Interoceptive Sensibility and Emotional Conceptualization for the Experience of Emotions
(2021)
The theory of constructed emotions suggests that different psychological components, including core affect (mental and neural representations of bodily changes), and conceptualization (meaning-making based on prior experiences and semantic knowledge), are involved in the formation of emotions. However, little is known about their role in experiencing emotions. In the current study, we investigated how individual differences in interoceptive sensibility and emotional conceptualization (as potential correlates of these components) interact to moderate three important aspects of emotional experiences: emotional intensity (strength of emotion felt), arousal (degree of activation), and granularity (ability to differentiate emotions with precision). To this end, participants completed a series of questionnaires assessing interoceptive sensibility and emotional conceptualization and underwent two emotion experience tasks, which included standardized material (emotion differentiation task; ED task) and self-experienced episodes (day reconstruction method; DRM). Correlational analysis showed that individual differences in interoceptive sensibility and emotional conceptualization were related to each other. Principal Component Analysis (PCA) revealed two independent factors that were referred to as sensibility and monitoring. The Sensibility factor, interpreted as beliefs about the accuracy of an individual in detecting internal physiological and emotional states, predicted higher granularity for negative words. The Monitoring factor, interpreted as the tendency to focus on the internal states of an individual, was negatively related to emotional granularity and intensity. Additionally, Sensibility scores were more strongly associated with greater well-being and adaptability measures than Monitoring scores. Our results indicate that independent processes underlying individual differences in interoceptive sensibility and emotional conceptualization contribute to emotion experiencing.
The Role of Interoceptive Sensibility and Emotional Conceptualization for the Experience of Emotions
(2021)
The theory of constructed emotions suggests that different psychological components, including core affect (mental and neural representations of bodily changes), and conceptualization (meaning-making based on prior experiences and semantic knowledge), are involved in the formation of emotions. However, little is known about their role in experiencing emotions. In the current study, we investigated how individual differences in interoceptive sensibility and emotional conceptualization (as potential correlates of these components) interact to moderate three important aspects of emotional experiences: emotional intensity (strength of emotion felt), arousal (degree of activation), and granularity (ability to differentiate emotions with precision). To this end, participants completed a series of questionnaires assessing interoceptive sensibility and emotional conceptualization and underwent two emotion experience tasks, which included standardized material (emotion differentiation task; ED task) and self-experienced episodes (day reconstruction method; DRM). Correlational analysis showed that individual differences in interoceptive sensibility and emotional conceptualization were related to each other. Principal Component Analysis (PCA) revealed two independent factors that were referred to as sensibility and monitoring. The Sensibility factor, interpreted as beliefs about the accuracy of an individual in detecting internal physiological and emotional states, predicted higher granularity for negative words. The Monitoring factor, interpreted as the tendency to focus on the internal states of an individual, was negatively related to emotional granularity and intensity. Additionally, Sensibility scores were more strongly associated with greater well-being and adaptability measures than Monitoring scores. Our results indicate that independent processes underlying individual differences in interoceptive sensibility and emotional conceptualization contribute to emotion experiencing.