A face to remember: emotional expression modulates prefrontal activity during memory formation

Emotion can exert a modulatory role on episodic memory. Several studies have shown that negative stimuli (e.g., words, pictures) are better remembered than neutral ones. Although facial expressions are powerful emotional stimuli and have been shown to influence perception and attention processes, little is known about their effect on memory. We used functional magnetic resonance imaging (fMRI) in humans to investigate the effects of expression (happy, neutral, and fearful) on prefrontal cortex (PFC) activity during the encoding of faces, using a subsequent memory effect paradigm. Our results show that activity in right PFC predicted memory for faces, regardless of expression, while a homotopic region in the left hemisphere was associated with successful encoding only for faces with an emotional expression. These findings are consistent with the proposed role of right dorsolateral PFC in successful encoding of nonverbal material, but also suggest that left DLPFC may be a site where integration of memory and emotional processes occurs. This study sheds new light on the current controversy regarding the hemispheric lateralization of PFC in memory encoding.     

Valence-specific regulation effects in a working memory task with emotional context

The modulatory effects of emotional context on episodic memory have been shown recently. We were interested whether working memory is similarly susceptible to emotional context or whether working memory helps to distract from emotion, i.e. serves to downregulate emotional reactions in order to sustain the prior intention. We tested the effects of emotional stimulation during active maintenance of information by modulating the emotional context of maintenance processes in a Sternberg item recognition task with two load conditions. Behavioral data revealed no impairment of working memory performance during emotional context. Actually, behavioral performance was better for emotional compared to neutral context during high load. Furthermore, emotional context had no interference effect on working memory-related brain activation. Instead, we found a valence-specific regulation effect: High cognitive effort was associated with reduced activity in emotion processing regions, i.e. the amygdala and ventral striatum. This effect was mediated by different prefrontal regions, i.e. by left inferior PFC for negative and left superior PFC for positive valence. Furthermore, our results reveal an integration effect of emotion and cognition in right dorsolateral prefrontal cortex showing increased recruitment with increasing complexity of the task. The results presented here are of relevance for the understanding of regulatory mechanisms and diseases characterized by increased susceptibility to emotional distraction.     

情绪加工中唤醒度的作用功能磁共振成像研究

目的通过检测参与情绪性图片编码加工相应激活脑区,探讨不同情绪唤醒度所涉及的特异性神经机制。方法20名健康被试,视觉呈现彩色高、中、低情绪唤醒度情景图片,要求对图片进行情绪强度判断,同时实时fMRI扫描,利用SPM2对功能数据进行ANOVA分析。结果高唤醒度主要激活杏仁核、海马、前额眶回和扣带回,而中唤醒度主要激活颞中回、前额背外侧、海马、额上回和枕部皮层。结论不同唤醒度情绪加工涉及不同的神经通路,杏仁核和前额叶不同亚区与情绪的唤醒程度有关。     

Contributions of stimulus valence and arousal to visual activation during emotional perception

Neuroimaging experiments have revealed that the visual cortex is involved in the processing of affective stimuli: seeing emotional pictures leads to greater activation than seeing neutral ones. It is unclear, however, whether such differential activation is due to stimulus valence or whether the results are confounded by arousal level. In order to investigate the contributions of valence and arousal to visual activation, we created a new category of "interesting" stimuli designed to have high arousal, but neutral valence, and employed standard neutral, unpleasant, and pleasant picture categories. Arousal ratings for pleasant and neutral pictures were equivalent, as were valence ratings for interesting and neutral pictures. Differential activation for conditions matched for arousal (pleasant vs neutral) as well as matched for valence (interesting vs neutral) indicated that both stimulus valence and arousal contributed to visual activation.     

Emotional context during encoding of neutral items modulates brain activation not only during encoding but also during recognition

In general, encoding of neutral material includes the context in which the respective material is learned. The effect of emotional context on successfully encoded neutral material has been investigated only recently in few studies, but the main underlying mechanisms are still fairly unknown. In the present study, we investigated the effect of positive and negative emotional context on encoding and later recognition of neutral items. We could demonstrate that brain activation not only during encoding but also during recognition of neutral items depended on the emotional valence of the encoding context. Whereas activation of medial temporal lobe structures during encoding specifically predicted subsequent memory when learning appears in a positive emotional context, activation of the anterior temporal cortex in a region with afferent input to the amygdala predicted memory for material learned in negative context. Recognition of items encoded in positive emotional context revealed activation of hippocampal and medial prefrontal regions, recognition of items encoded in negative emotional context revealed activation of the caudate nucleus. We assume that our findings reflect the recruitment of different brain circuits depending on the emotional context during learning.     

The modulation of pain by attention and emotion: A dissociation of perceptual and spinal nociceptive processes

Emotions and attention have been shown to influence the perception of pain and several psychophysiological studies have suggested an implication of descending modulatory mechanisms to explain these effects. However, the specificity of the neurophysiological mechanisms underlying the emotional and attentional modulation of pain still remains unclear. In order to differentiate the supra‐spinal and spinal mechanisms involved in emotional and attentional modulation of pain, we measured pain perception (self‐ratings) and the RIII reflex in healthy volunteers during the presentation of pleasant, unpleasant and neutral pictures, as well as during a baseline condition with no visual distractor (Experiment 1). In a second experiment, we manipulated the emotional arousal induced by pleasant and unpleasant pictures in order to compare more directly the effects of distraction and arousal. Whereas emotional valence influenced pain and the amplitude of the RIII reflex in the same direction (negative>positive), distraction by neutral pictures reduced pain but increased the RIII reflex relative to baseline. Increased arousal further potentiated the effects of negative valence on both pain and the RIII reflex and the effects of positive emotions on pain, as previously reported. However, arousal did not potentiate the inhibitory effect of positive pictures on the RIII and seems insufficient to account for the effect of distraction on the RIII. Overall, these data provide further evidence that attention and emotion modulate pain through partially dissociable neurophysiological mechanisms.     

Emotional control of nociceptive reactions (ECON): Do affective valence and arousal play a role?

Prior research suggests emotional picture-viewing modulates motoric (nociceptive flexion reflex), autonomic (skin conductance response, heart rate acceleration), and subjective (pain rating) reactions to noxious electrodermal stimulation. The present study sought to determine whether emotional valence and arousal contribute to nociception modulation. To do so, pictures varying in emotional content (erotica, food, neutral, loss, attack) were chosen to manipulate emotional valence (pleasant=erotic and food; unpleasant=loss and attack) and arousal (low=food and loss; moderate=erotica and attack). Pictures were presented in pseudorandom order to elicit emotional processing while noxious electric stimulations were delivered to the sural nerve. Nociceptive flexion reflex (NFR) magnitude, skin conductance response (SCR), heart rate (HR) acceleration, and subjective pain ratings to each stimulation were measured, standardized, averaged by picture content, and analyzed. Results suggested that picture-viewing explained 52% of the variance in the multivariate combination of the nociceptive reactions and modulated them in parallel. Pleasant pictures inhibited reactions, whereas unpleasant pictures enhanced them. However, only erotica and attack pictures elicited significant modulation relative to neutral pictures, suggesting arousal also contributed. An exploratory multilevel analysis also supported this conclusion. Together, these data suggest emotional control of nociceptive reactions (ECON) is associated with a valence-by-arousal interaction. Implications of these findings for how emotional picture-viewing can be used to study supraspinal modulation are discussed.     

Neural mechanisms underlying the integration of emotion and working memory

The present study aimed at investigating the behavioral effects and neuronal correlates of emotional content and emotional components, i.e. valence and arousal, in the context of a verbal working memory task. Our findings in twenty healthy male subjects demonstrate that (1) word valence has no impact on performance in the verbal working memory task, and (2) that emotion leads to an increase of activation in cognition-related lateral prefrontal regions, whereas cognitive effort yields enhanced deactivation in emotion-related cortical midline regions. The stronger dorsolateral prefrontal recruitment during emotional stimuli may reflect an arousal effect or higher cognitive effort due to interference with emotion.     

Decoding the neural representation of affective states

Brain activity was monitored while participants viewed picture sets that reflected high or low levels of arousal and positive, neutral, or negative valence. Pictures within a set were presented rapidly in an incidental viewing task while fMRI data were collected. The primary purpose of the study was to determine if multi-voxel pattern analysis could be used within and between participants to predict valence, arousal and combined affective states elicited by pictures based on distributed patterns of whole brain activity. A secondary purpose was to determine if distributed patterns of whole brain activity can be used to derive a lower dimensional representation of affective states consistent with behavioral data. Results demonstrated above chance prediction of valence, arousal and affective states that was robust across a wide range of number of voxels used in prediction. Additionally, individual differences multidimensional scaling based on fMRI data clearly separated valence and arousal levels and was consistent with a circumplex model of affective states.     

How mood challenges emotional memory formation: an fMRI investigation

Experimental mood manipulations and functional magnetic resonance imaging (fMRI) provide a unique opportunity for examining the neural correlates of mood-congruent memory formation. While prior studies in mood-disorder patients point to the medial temporal lobe in the genesis of mood-congruent memory (MCM) bias, the interaction between mood and emotional memory formation has not been investigated in healthy participants. In particular it remains unclear how regulatory structures in the pre-frontal cortex may be involved in mediating this phenomenon. In this study, event-related fMRI was performed on 20 healthy participants using a full-factorial, within-subjects repeated-measures design to examine how happy and sad moods impact memory for valenced stimuli (positive, negative and neutral words). Main effects of mood, stimulus valence and memory were examined as was activity related to successful memory formation during congruent and in-congruent moods. Behavioral results confirm an MCM bias while imaging results show amygdala and hippocampal engagement in a global mood and successful recall, respectively. MCM formation was characterized by increased activity during mood-congruent encoding of negative words in the orbito-frontal cortex (OFC) and for mood-incongruent processing of negative words in medial- and inferior-frontal gyri (MFG/IFG). These findings indicate that different pre-frontal regions facilitate mood-congruent and incongruent encoding of successfully recalled negative words at the time of learning, with OFC enhancing congruency and the left IFG and MFG helping overcome semantic incongruities between mood and stimulus valence.     

Noradrenaline mediates amygdala activation in men and women during encoding of emotional material

The amygdala is a pivotal structure in humans for encoding of emotional information, as shown by recent imaging studies. It is unknown which neurotransmitters are specifically involved in the human amygdala, although in animal studies noradrenaline was shown to be essential. In our study, participants received the betablocker propranolol (which blocks the noradrenergic response) or placebo when watching neutral to highly negative arousing pictures. Amygdala activation, monitored with functional magnetic resonance imaging (fMRI), increased with emotional intensity of the pictures under placebo condition. Betablockade selectively decreased amygdala activation for emotional pictures of the second highest category, but not for the highest or lower (neutral) category pictures. Two findings add to the existing knowledge in this area. First, the activation pattern in the amygdala under placebo condition shows a nonlinearity related to the emotional categories of the pictures. Second, propranolol disturbs this activation pattern in the amygdala. Explorations with respect to gender show a similar effect of betablockade on amygdala activation in both men and women, but a difference in its effect on long-term memory for emotional pictures. This study supports the hypothesis that the neurotransmitter noradrenaline also mediates amygdala activity in humans when processing emotional stimuli and that betablockers can disrupt the normal activation pattern in the amygdala.     

情绪记忆对精神分裂症患者风险决策的影响

目的 探讨情绪记忆对精神分裂症患者风险决策能力的影响.方法 精神分裂症患者（SC组）40例和健康对照（HC组）40例,采用情绪记忆和风险决策两方面的实验任务,比较两组情绪记忆的结果和执行风险决策的能力.结果 两组情绪图片的评分差异无统计学意义（P〉0.05）,对负性和中性图片的回忆率差异均有统计学意义（t=-4.44,P〈0.01;t=-3.32,P〈0.01）;与HC组比较,SC组在奖赏后和惩罚后的风险选择频率均显著升高（t=-2.29,P〈0.05;t=-6.18,P〈0.01）.结论 精神分裂症患者追求高奖赏,惩罚后风险选择的抑制效应消失,且患者风险决策能力的损害与其情绪记忆功能受损密切相关.     

Emotion suppression reduces hippocampal activity during successful memory encoding

People suppressing their emotions while facing an emotional event typically remember it less well. However, the neural mechanisms underlying the impairing effect of emotion suppression on successful memory encoding are not well understood. Because successful memory encoding relies on the hippocampus and the amygdala, we hypothesized that memory impairments due to emotion suppression are associated with down-regulated activity in these brain areas. 59 healthy females were instructed either to simply watch the pictures or to down-regulate their emotions by using a response-focused emotion suppression strategy. Brain activity was recorded using functional magnetic resonance imaging (fMRI), and free recall of pictures was tested afterwards. As expected, suppressing one's emotions resulted in impaired recall of the pictures. On the neural level, the memory impairments were associated with reduced activity in the right hippocampus during successful encoding. No significant effects were observed in the amygdala. In addition, functional connectivity between the hippocampus and the right dorsolateral prefrontal cortex was strongly reduced during emotion suppression, and these reductions predicted free-recall performance. Our results indicate that emotion suppression interferes with memory encoding on the hippocampal level, possibly by decoupling hippocampal and prefrontal encoding processes, suggesting that response-focused emotion suppression might be an adaptive strategy for impairing hippocampal memory formation in highly arousing situations.     

Distinguishing specific sexual and general emotional effects in fMRI-subcortical and cortical arousal during erotic picture viewing

Sexual activity involves excitement with high arousal and pleasure as typical features of emotions. Brain activations specifically related to erotic feelings and those related to general emotional processing are therefore hard to disentangle. Using fMRI in 21 healthy subjects (11 males and 10 females), we investigated regions that show activations specifically related to the viewing of sexually intense pictures while controlling for general emotional arousal (GEA) or pleasure. Activations in the ventral striatum and hypothalamus were found to be modulated by the stimulus' specific sexual intensity (SSI) while activations in the anterior cingulate cortex were associated with an interaction between sexual intensity and emotional valence. In contrast, activation in other regions like the dorsomedial prefrontal cortex, the mediodorsal thalamus and the amygdala was associated only with a general emotional component during sexual arousal. No differences were found in these effects when comparing females and males. Our findings demonstrate for the first time neural differentiation between emotional and sexual components in the neural network underlying sexual arousal.     

Motivated attention in emotional picture processing is reflected by activity modulation in cortical attention networks

In the present study, we presented high (pleasant and unpleasant)- and low (neutral)-arousing emotional pictures in a steady state visual evoked field paradigm while recording the magnetoencephalogram. Applying a minimum norm estimation (MNE) technique, we determined the origin and the strength of the evoked neuromagnetic field. In addition to magnetocortical data, we examined subjective ratings, heart rate change and viewing time to obtain a multivariate data base of emotional experience related to the present paradigm. As evidenced by the MNE, pictures rated as high arousing elicited greater activity in frontoparietal cortical networks than low-arousing pictures, with a right hemispheric predominance. This effect was also observed in occipito-temporal regions but to a lesser extent. Longer viewing times for high-arousing pictures and sustained heart rate deceleration for high-arousing unpleasant pictures indicated that these stimuli were of high motivational relevance compared to neutral pictures. Taken together, we argue that activity in higher-order frontoparietal cortical attention networks is modulated by emotional arousal. In turn, this attention network influences activity in systems performing stimulus processing.     

Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance

Much research demonstrates that emotional stimuli prompt increased amygdala and visual cortical activation. Here we measure functional activity in the visual cortex and amygdala with fMRI while selected fearful and control participants view a range of neutral, emotionally arousing, and fear-relevant pictures. BOLD signal in the amygdala and inferotemporal visual cortex closely covaried during emotional picture viewing, increasing systematically with rated picture arousal. Furthermore, fearful individuals reacting to specific fear cues show parallel, heightened activation in these two structures compared with non-fearful controls. The findings suggest an individually-sensitive, positive linear relationship between the arousing quality of visual stimuli and activation in amygdala and ventral visual cortex, supporting the hypothesized functional connectivity described in the animal model.     

fMRI correlates of the episodic retrieval of emotional contexts

Functional neuroimaging studies reveal differences in neural correlates of the retrieval of emotional and nonemotional memories. In the present experiment, encoding of emotionally neutral pictures in association with positively, neutrally or negatively valenced background contexts led to differential modulation of neural activity elicited in a subsequent recognition memory test for these pictures. Recognition of stimuli previously studied in emotional compared to neutral contexts elicited enhanced activity in structures previously implicated in episodic memory, including the parahippocampal cortex, hippocampus and prefrontal cortex. In addition, there was engagement of structures linked more specifically to emotional processing, including the amygdala, orbitofrontal cortex and anterior cingulate cortex. These emotion-related effects displayed both valence-independent and valence-specific components. We discuss the findings in terms of current models of emotional memory retrieval.     

Affective pain modulation in fibromyalgia,somatoform pain disorder,back pain,and healthy controls

Previous research suggested that patients with fibromyalgia (FM) experience a higher pain intensity (clinical pain) than do patients with musculoskeletal pain after negative emotional priming compared to positive priming. To further examine affective pain modulation in FM, we applied an experimental pain induction to compare 30 patients with FM with 30 healthy (pain‐free) participants (HC), and 30 patients with back pain (BP). For another group of 30 patients with somatoform pain disorder (SF), we predicted the same pain modulation as for FM. As primes we presented positive, neutral, negative, and pain‐related pictures and assessed pain intensity in response to a fixed pressure weight. Overall, picture valence modulated pain intensities (in the order of pain‐related>negative pictures>neutral), but the pain intensities between neutral and positive pictures did not differ significantly. SF reported significantly higher pain intensities than did BP and HC; FM were in between, but did not differ significantly from the three other groups. There was no interaction of priming and group. Affective modulation of pain was not specifically altered in FM and SF, but SF were more sensitive to pressure pain than BP and HC.