Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding

Emotionally arousing experiences are usually well retained, an effect that depends on the release of adrenal stress hormones. Animal studies have shown that corticosterone and noradrenaline – representing the two main stress hormone systems – act in concert to enhance memory formation by actions involving the amygdala, hippocampus and prefrontal cortex (PFC). Here we test whether interactions between these two stress hormone systems also affect human memory formation as well as the associated pattern of brain activation. To this end, forty-eight male human subjects received hydrocortisone, yohimbine or both before presentation of emotional and neutral pictures. Activity in the amygdala, hippocampus and PFC was monitored with functional Magnetic Resonance Imaging (fMRI) during encoding of these stimuli, when hormonal levels were elevated. Memory performance was tested 1 week later. We investigated whether an increased level of one of the two hormone systems would lead to differential effects compared to the combined application of the drugs on brain activation and memory performance. We report that the application of cortisol led to an overall enhancing effect on recognition memory, with no significant additional effect of yohimbine. However, during encoding the brain switched from amygdala/hippocampus activation with either hormone alone, to a strong deactivation of prefrontal areas under the influence of the combination of both exogenous hormones. Although we did not find evidence that exogenous stimulation of the noradrenergic and corticosteroid systems led to significant interaction effects on memory performance in this experiment, we conclude that stress hormone levels during encoding did differentially determine the activation pattern of the brain circuits here involved.     

The role of the noradrenergic system in emotional memory

This contribution is an overview on the role of noradrenaline as neurotransmitter and stress hormone in emotional memory processing. The role of stress hormones in memory formation of healthy subjects can bear significance for the derailment of memory processes, for example, in post traumatic stress disorder (PTSD). Increased noradrenaline levels lead to better memory performance, whereas blocking the noradrenergic receptors with a betablocker attenuates this enhanced memory for emotional information. Noradrenaline appears to interact with cortisol in emotional memory processes, varying from encoding to consolidation and retrieval. Imaging studies show that confronting human subjects with emotional stimuli results in increased amygdala activation and that this activation is noradrenergic dependent. The role of noradrenaline in other brain areas, such as hippocampus and prefrontal cortex, is shortly summarized. Finally, the pros and cons of a therapeutic application of betablockers in the (secondary) prevention of PTSD will be discussed.     

7～10岁自闭症谱系障碍儿童对情绪面孔的觉察与加工

为了考察自闭症谱系障碍(autism spectrum disorder,ASD)儿童对不同情绪面孔的觉察和加工情况,设计两个眼动实验任务,要求14名7～10岁ASD儿童和20名同年龄正常儿童观看图片。实验一采用将情绪面孔嵌入风景图片中引起语义不一致的刺激;实验二采用含有情绪面孔的无意义背景乱序图片刺激。结果发现:(1)ASD儿童对不同情绪面孔的觉察时间都显著长于正常儿童;(2)与正常儿童一样,ASD儿童表现出对恐惧面孔的注意偏向;(3)实验二中,ASD儿童对不同情绪面孔内部特征区的注意分配与正常儿童不同;正常儿童能注意最能展示该类情绪特征信息的区域,如恐惧的眼睛、愉快的嘴巴,而ASD儿童对三类情绪面孔特征区的注意分配方式相似;(4)两个实验条件下,ASD者对不同情绪面孔的觉察、加工模式与正常儿童相似。     

Amygdala responses to emotionally valenced stimuli in older and younger adults

Abstract— As they age, adults experience less negative emotion, come to pay less attention to negative than to positive emotional stimuli, and become less likely to remember negative than positive emotional materials. This profile of findings suggests that, with age, the amygdala may show decreased reactivity to negative information while maintaining or increasing its reactivity to positive information. We used event-related functional magnetic resonance imaging to assess whether amygdala activation in response to positive and negative emotional pictures changes with age. Both older and younger adults showed greater activation in the amygdala for emotional than for neutral pictures; however, for older adults, seeing positive pictures led to greater amygdala activation than seeing negative pictures, whereas this was not the case for younger adults.     

Neural circuitry of emotion regulation: Effects of appraisal,attention, and cortisol administration

Psychosocial well-being requires effective regulation of emotional responding in context of threat or stress. Neuroimaging studies have focused on instructed, volitional regulation (e.g., reappraisal or distancing), largely ignoring implicit regulation that does not involve purposeful effort to alter emotional experience. These implicit processes may or may not involve the same neural pathways as explicit regulatory strategies. We examined the neurobiology of implicit emotional regulation processes and the impact of the stress hormone cortisol on these processes. Our study task employed composite pictures of faces and places to examine neural activity during implicit emotional processing (of emotional faces), while these responses were implicitly regulated by attention shift away from the emotionally evocative stimuli, and while subjects reflectively appraised their own emotional response to them. Subjects completed the task in an fMRI scanner after random assignment to receive placebo or hydrocortisone (HCT), an orally administered version of cortisol. Implicit emotional processing activated insula/IFG, dACC/dMPFC, midbrain and amygdala. With attention shifting, we saw diminished signal in emotion generating/response regions (e.g., amygdala) and increased activations in task specific attention regions like parahippocampus. With appraisal of emotions, we observed robust activations in medial prefrontal areas, where activation is also seen in instructed reappraisal studies. We observed no main effects of HCT administration on brain, but males and females showed opposing neural effects in prefrontal areas. The data suggest that different types of emotion regulation utilize overlapping circuits, but with some strategy specific activation. Further study of the dimorphic sex response to cortisol is needed.     

Verbal and Nonverbal Emotional Memory Following Unilateral Amygdala Damage

The amygdala is involved in the normal facilitation of memory by emotion, but the separate contributions of the left and right amygdala to memory for verbal or nonverbal emotional material have not been investigated. Fourteen patients with damage to the medial temporal lobe including the amygdala (seven left, seven right), 18 brain-damaged, and 36 normal controls were exposed to emotional and neutral pictures accompanied by verbal narratives. Memory for both narratives and pictures was assessed with a free recall test 24 h later. Subjects with left amygdala damage failed to show the normally robust enhancement of memory for verbal and nonverbal emotional stimuli. The group with right amygdala damage showed the normal pattern of facilitation of memory by emotion for both verbal and nonverbal stimuli despite an overall reduction in memory performance. Furthermore, subjects with left amygdala damage were disproportionately impaired on memory for emotional narratives as compared with memory for emotional pictures. The latter finding offers partial support for a lateralized and material-specific pattern of the amygdala's contribution to emotional memory.     

Gaze Patterns When Looking at Emotional Pictures: Motivationally Biased Attention

Pictures of either emotionally neutral, pleasant (affectionate), or unpleasant (threat and injury) scenes were paired with nonemotional control pictures and presented for 3 s, while eye fixations were monitored. Preferential attention to the emotional picture of eah pair occurred at an early processing stage: The probability of placement of the first fixation and the proportion of viewing time during the first 500 ms were higher for both pleasant and unpleasant pictures than for neutral pictures, whereas later fixation location and time were not differentially affected. This suggests that, when emotional and nonemotional stimuli are presented simultaneously, emotional meaning captures initial overt orienting and engages attention early, as measured by gaze direction and duration. The possibility that this effect could be accounted for by perceptual differences—such as luminance and complexity—between emotional and neutral pictures was ruled out.     

Event-related potentials of emotional memory: encoding pleasant,unpleasant, and neutral pictures

Emotional events tend to be remembered better than nonemotional events. We investigated this phenomenon by measuring two event-related potential (ERP) effects: the emotion effect (more positive ERPs for pleasant or unpleasant stimuli than for neutral stimuli) and the subsequent memory effect (more positive ERPs for subsequently remembered items than for subsequently forgotten items). ERPs were measured while subjects rated the emotional content of pleasant, unpleasant, and neutral pictures. As was expected, subsequent recall was better for pleasant and unpleasant pictures than for neutral pictures. The emotion effect was sensitive to arousal in parietal electrodes and to both arousal and valence in frontocentral electrodes. The subsequent memory effect at centroparietal electrodes was greater for emotional pictures than for neutral pictures during an early epoch (400-600 msec). This result suggests that emotional information has privileged access to processing resources, possibly leading to better memory formation.     

What kind of mood influences what kind of memory: The role of arousal and information structure

Mood-congruent memory was investigated as a function of the structure of the information to be remembered (categorical vs. isolated) and the participant’s arousal (stimulating drug vs. placebo). Free recall of photographs showing either pleasant or unpleasant scenes was assessed for subjects under positive or neutral mood states, induced by the imagination of emotional experiences under relaxation. Although the arousal manipulation did not affect the recall performance, the findings highlight the importance of the information structure: a mood-congruency effect was obtained for the isolated pictures; however, the effect did not appear for categorical material, suggesting that structural constraints on the recall process can override the influence of mood on memory. Interestingly, the subject’s evaluations of the pictures also shifted toward their mood states. A general recall advantage of positive mood was observed.     

Electrophysiological differences in the processing of affective information in words and pictures

It is generally assumed that affective picture viewing is related to higher levels of physiological arousal than is the reading of emotional words. However, this assertion is based mainly on studies in which the processing of either words or pictures has been investigated under heterogenic conditions. Positive, negative, relaxing, neutral, and background (stimulus fragments) words and pictures were presented to subjects in two experiments under equivalent experimental conditions. In Experiment 1, neutral words elicited an enhanced late positive component (LPC) that was associated with an increased difficulty in discriminating neutral from background stimuli. In Experiment 2, high-arousing pictures elicited an enhanced early negativity and LPC that were related to a facilitated processing for these stimuli. Thus, it seems that under some circumstances, the processing of affective information captures attention only with more biologically relevant stimuli. Also, these data might be better interpreted on the basis of those models that postulate a different access to affective information for words and pictures.     

Emotional memories are not all created equal: evidence for selective memory enhancement

Human brain imaging studies have shown that greater amygdala activation to emotional relative to neutral events leads to enhanced episodic memory. Other studies have shown that fearful faces also elicit greater amygdala activation relative to neutral faces. To the extent that amygdala recruitment is sufficient to enhance recollection, these separate lines of evidence predict that recognition memory should be greater for fearful relative to neutral faces. Experiment 1 demonstrated enhanced memory for emotionally negative relative to neutral scenes; however, fearful faces were not subject to enhanced recognition across a variety of delays (15 min to 2 wk). Experiment 2 demonstrated that enhanced delayed recognition for emotional scenes was associated with increased sympathetic autonomic arousal, indexed by the galvanic skin response, relative to fearful faces. These results suggest that while amygdala activation may be necessary, it alone is insufficient to enhance episodic memory formation. It is proposed that a sufficient level of systemic arousal is required to alter memory consolidation resulting in enhanced recollection of emotional events.     

Mapping the apetitive and aversive systems with emotional pictures using a block-design fMRI procedure

Negative emotional pictures from the International Affective Pictures System (IAPS) have been successful in mapping brain areas related to the aversive system. However, the capacity of positive emotional pictures to study the brain areas related to the appetitive system (i.e., nucleus accumbens, prefrontal cortex) is less established. In this study, we used a block fMRI design to investigate this issue, including emotional pictures as background while participants performed a vowel-consonant discrimination task. Importantly, participants were heterosexual males and all positive pictures were related to erotic couples, opposite-sex erotica, or romantic scenes. Negative pictures were similar to those used in previous studies. Results were consistent with previous studies using event-related designs, showing activation of amygdala, lateral prefrontal cortex, and occipito-temporal areas, but positive pictures showed a significant activation in the left nucleus accumbens. These findings provide evidence of the utility of block designs in emotional research (positive emotional pictures).     

Time course of attentional bias to emotional scenes in anxiety: Gaze direction and duration

Pictures of emotionally neutral, positive, and negative (threat- or harm-related) scenes were presented for 3 seconds, paired with nonemotional control pictures. The eye fixations of high and low trait anxiety participants were monitored. Intensity of stimulus emotionality was varied, with two levels of perceptual salience for each picture (colour vs. greyscale). Regardless of perceptual salience, high anxiety was associated with preferential attention: (a) towards all types of emotional stimuli in initial orienting, as revealed by a higher probability of first fixation on the emotional picture than on the neutral picture of a pair; (b) towards positive and harm stimuli in a subsequent stage of early engagement, as shown by longer viewing times during the first 500 ms following onset of the pictures; and with (c) attention away from (i.e., avoidance) harm stimuli in a later phase, as indicated by shorter viewing times and lower frequency of fixation during the last 1000 ms of picture exposure. This suggests that the nature of the attentional bias varies as a function of the time course in the processing of emotional pictures.     

Time course of attentional bias to emotional scenes in anxiety: Gaze direction and duration

Pictures of emotionally neutral, positive, and negative (threat‐ or harm‐related) scenes were presented for 3 seconds, paired with nonemotional control pictures. The eye fixations of high and low trait anxiety participants were monitored. Intensity of stimulus emotionality was varied, with two levels of perceptual salience for each picture (colour vs. greyscale). Regardless of perceptual salience, high anxiety was associated with preferential attention: (a) towards all types of emotional stimuli in initial orienting, as revealed by a higher probability of first fixation on the emotional picture than on the neutral picture of a pair; (b) towards positive and harm stimuli in a subsequent stage of early engagement, as shown by longer viewing times during the first 500 ms following onset of the pictures; and with (c) attention away from (i.e., avoidance) harm stimuli in a later phase, as indicated by shorter viewing times and lower frequency of fixation during the last 1000 ms of picture exposure. This suggests that the nature of the attentional bias varies as a function of the time course in the processing of emotional pictures.     

Enhanced recognition of emotional stimuli in the chimpanzee (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

Humans often have a better memory of emotional events than neutral events. From the comparative-cognitive perspective, we explored the enhancement of recognition memory by emotion in chimpanzees (Pan troglodytes) using a serial probe recognition task. In this task, we sequentially presented a list of pictures to subjects and then tested their recognition of specific pictures from within the list. We selected pictures of aggressive chimpanzees as emotional stimuli and less tensed, relaxed chimpanzees as neutral stimuli. In Experiment 1, we gave four-item lists to two young chimpanzees; one showed significantly greater recognition of pictures depicting aggressive chimpanzees than neutral ones. In Experiment 2, this chimpanzee was further tested using a recognition task with eight-item lists. The subject again showed better recognition of emotional stimuli than neutral. Furthermore, the presence of an emotional stimulus in the list also facilitated recognition of the neutral item immediately following it. Overall, although only one of the two chimpanzees showed enhanced recognition memory by emotional stimuli, this is the first demonstration of such a response in the chimpanzee. The findings are discussed in comparison with those of human studies.     

情绪效价和唤醒对熟悉性和回想的不同影响

本研究检验了情绪的效价和唤醒对记忆提取阶段熟悉性过程和回想过程的影响及其心理机制。结果发现,编码阶段无分心任务时,积极图片的高、低自信再认准确率均高于消极图片,而唤醒对于高自信再认准确率的影响只限于消极图片;在编码阶段设置分心任务时,发现积极和消极的高唤醒图片的高自信再认准确率显著高于低唤醒图片。这些结果说明情绪的效价影响了熟悉性和回想两类记忆过程,而唤醒只影响回想过程,效价效应是编码阶段被试调用认知资源对积极图片进行精细加工的结果,而唤醒对回想过程的影响是自动编码高唤醒刺激细节的结果。     

情绪场景图片的注意偏向：眼动研究

注意实验中,与不带情绪色彩的刺激相比,具有情绪意义的刺激可引起注意偏向。本研究以情绪场景图片为材料,通过眼动技术分别记录被试在反向眼跳任务和Go/No-go任务中的眼动数据,考察了情绪图片的注意偏向。结果发现：反向眼跳任务中,对情绪图片的眼跳潜伏期比中性图片更长,眼跳错误率也更高;在Go任务中,相对于呈现在中央的中性图片,情绪图片引起的对靶子的眼跳潜伏期更长;在No-go任务中,相对于呈现在中央的中性图片,情绪图片引起的眼跳错误率更低。实验结果说明,情绪图片可引起注意偏向,表现为更快的捕获注意并且注意更难从情绪图片上转移。     

Eye movement assessment of selective attentional capture by emotional pictures

The eye-tracking method was used to assess attentional orienting to and engagement on emotional visual scenes. In Experiment 1, unpleasant, neutral, or pleasant target pictures were presented simultaneously with neutral control pictures in peripheral vision under instruction to compare pleasantness of the pictures. The probability of first fixating an emotional picture, and the frequency of subsequent fixations, were greater than those for neutral pictures. In Experiment 2, participants were instructed to avoid looking at the emotional pictures, but these were still more likely to be fixated first and gazed longer during the first-pass viewing than neutral pictures. Low-level visual features cannot explain the results. It is concluded that overt visual attention is captured by both unpleasant and pleasant emotional content.     

Immediate memory consequences of the effect of emotion on attention to pictures

Emotionally arousing stimuli are at once both highly attention grabbing and memorable. We examined whether emotional enhancement of memory (EEM) reflects an indirect effect of emotion on memory, mediated by enhanced attention to emotional items during encoding. We tested a critical prediction of the mediation hypothesis-that regions conjointly activated by emotion and attention would correlate with subsequent EEM. Participants were scanned with fMRI while they watched emotional or neutral pictures under instructions to attend to them a lot or a little, and were then given an immediate recognition test. A region in the left fusiform gyrus was activated by emotion, voluntary attention, and subsequent EEM. A functional network, different for each attention condition, connected this region and the amygdala, which was associated with emotion and EEM, but not with voluntary attention. These findings support an indirect cortical mediation account of immediate EEM that may complement a direct modulation model.     

No emotional "pop-out" effect in natural scene viewing

It has been shown that attention is drawn toward emotional stimuli. In particular, eye movement research suggests that gaze is attracted toward emotional stimuli in an unconscious, automated manner. We addressed whether this effect remains when emotional targets are embedded within complex real-world scenes. Eye movements were recorded while participants memorized natural images. Each image contained an item that was either neutral, such as a bag, or emotional, such as a snake or a couple hugging. We found no latency difference for the first target fixation between the emotional and neutral conditions, suggesting no extrafoveal "pop-out" effect of emotional targets. However, once detected, emotional targets held attention for a longer time than neutral targets. The failure of emotional items to attract attention seems to contradict previous eye-movement research using emotional stimuli. However, our results are consistent with studies examining semantic drive of overt attention in natural scenes. Interpretations of the results in terms of perceptual and attentional load are provided.