Effects of Aging on Functional Connectivity of the Amygdala for Subsequent Memory of Negative Pictures: A Network Analysis of Functional Magnetic Resonance Imaging Data

ABSTRACT— Aging is associated with preserved enhancement of emotional memory, as well as with age-related reductions in memory for negative stimuli, but the neural networks underlying such alterations are not clear. We used a subsequent-memory paradigm to identify brain activity predicting enhanced emotional memory in young and older adults. Activity in the amygdala predicted enhanced emotional memory, with subsequent-memory activity greater for negative stimuli than for neutral stimuli, across age groups, a finding consistent with an overall enhancement of emotional memory. However, older adults recruited greater activity in anterior regions and less activity in posterior regions in general for negative stimuli that were subsequently remembered. Functional connectivity of the amygdala with the rest of the brain was consistent with age-related reductions in memory for negative stimuli: Older adults showed decreased functional connectivity between the amygdala and the hippocampus, but increased functional connectivity between the amygdala and dorsolateral prefrontal cortices. These findings suggest that age-related differences in the enhancement of emotional memory might reflect decreased connectivity between the amygdala and typical subsequent-memory regions, as well as the engagement of regulatory processes that inhibit emotional responses.     

Differentiating emotional processing and attention in psychopathy with functional neuroimaging

Individuals with psychopathy are often characterized by emotional processing deficits, and recent research has examined the specific contexts and cognitive mechanisms that underlie these abnormalities. Some evidence suggests that abnormal features of attention are fundamental to emotional deficits in persons with psychopathy, but few studies have demonstrated the neural underpinnings responsible for such effects. Here, we use functional neuroimaging to examine attention–emotion interactions among incarcerated individuals (n = 120) evaluated for psychopathic traits using the Hare Psychopathy Checklist–Revised (PCL-R). Using a task designed to manipulate attention to emotional features of visual stimuli, we demonstrate effects representing implicit emotional processing, explicit emotional processing, attention-facilitated emotional processing, and vigilance for emotional content. Results confirm the importance of considering mechanisms of attention when evaluating emotional processing differences related to psychopathic traits. The affective-interpersonal features of psychopathy (PCL-R Factor 1) were associated with relatively lower emotion-dependent augmentation of activity in visual processing areas during implicit emotional processing, while antisocial-lifestyle features (PCL-R Factor 2) were associated with elevated activity in the amygdala and related salience network regions. During explicit emotional processing, psychopathic traits were associated with upregulation in the medial prefrontal cortex, insula, and superior frontal regions. Isolating the impact of explicit attention to emotional content, only Factor 1 was related to upregulation of activity in the visual processing stream, which was accompanied by increased activity in the angular gyrus. These effects highlight some important mechanisms underlying abnormal features of attention and emotional processing that accompany psychopathic traits.     

Putting feelings into words: affect labeling disrupts amygdala activity in response to affective stimuli

Putting feelings into words (affect labeling) has long been thought to help manage negative emotional experiences; however, the mechanisms by which affect labeling produces this benefit remain largely unknown. Recent neuroimaging studies suggest a possible neurocognitive pathway for this process, but methodological limitations of previous studies have prevented strong inferences from being drawn. A functional magnetic resonance imaging study of affect labeling was conducted to remedy these limitations. The results indicated that affect labeling, relative to other forms of encoding, diminished the response of the amygdala and other limbic regions to negative emotional images. Additionally, affect labeling produced increased activity in a single brain region, right ventrolateral prefrontal cortex (RVLPFC). Finally, RVLPFC and amygdala activity during affect labeling were inversely correlated, a relationship that was mediated by activity in medial prefrontal cortex (MPFC). These results suggest that affect labeling may diminish emotional reactivity along a pathway from RVLPFC to MPFC to the amygdala.     

Emotion regulation and amygdala-precuneus connectivity: Focusing on attentional deployment

Attentional deployment is an emotion regulation strategy that involves shifting attentional focus. Deploying attention to non-arousing, compared to arousing, regions of unpleasant images has been associated with reduced negative affect, reduced amygdala activation, and increased activity in fronto-parietal control networks. The current study examined neural correlates and functional connectivity associated with using attentional deployment to increase negative affect (deploying attention towards arousing unpleasant information) or to decrease negative affect (deploying attention away from arousing unpleasant information), compared to naturally viewing unpleasant images, in 42 individuals while concurrently monitoring eye movements. Directing attention to both arousing and non-arousing regions resulted in enhanced fronto-parietal activation compared to natural viewing, but only directing attention to non-arousing regions was associated with changes in amygdala activation. There were no significant differences in connectivity between naturally viewing unpleasant images and focusing on arousing regions. However, naturally viewing unpleasant images, relative to focusing on non-arousing regions, was associated with increased connectivity between the amygdala and visual cortex, while focusing on non-arousing regions of unpleasant images, compared to natural viewing, was associated with increased connectivity between the amygdala and the precuneus. Amygdala-precuneus connectivity correlated positively with eye-tracking measures of attentional deployment success and with trait reappraisal. Deploying attention away from arousing unpleasant information, then, may depend upon functional relationships between the amygdala and parietal regions implicated in attentional control. Furthermore, these relationships might relate to the ability to successfully implement attentional deployment, and the predisposition to utilize adaptive emotion regulation strategies.     

Modulation of retrieval processing reflects accuracy of emotional source memory

There is considerable evidence that encoding and consolidation of memory are modulated by emotion, but the retrieval of emotional memories is not well characterized. Here we manipulated the emotional context with which affectively neutral stimuli were associated during encoding, allowing us to examine neural activity associated with retrieval of emotional memories without confounding the emotional attributes of cue items and the retrieved context. Using a source memory procedure we were also able to compare how retrieval processing was modulated when the emotional encoding context was recollected or not. An interaction between emotional encoding context and accuracy of source memory revealed that successful retrieval of emotional context was associated with activity in left amygdala, and a left frontotemporal network including anterior insula, prefrontal cortex and cingulate. In contrast, when contextual retrieval was unsuccessful, items encoded in emotional contexts elicited enhanced activity in right amygdala and a right-lateralized network that included extrastriate visual areas. These findings indicate distinct effects of emotion on successful and unsuccessful retrieval of source information, including lateralization of amygdala responses.     

情绪加工中杏仁核的效价特异性

杏仁核是情绪信息加工的关键脑区。近年来心理学和神经科学领域发现了杏仁核情绪加工的效价特异性现象,并且整体存在左侧杏仁核对正性情绪、右侧杏仁核对负性情绪以及双侧杏仁核负性偏好的特异性趋势,且受到材料突出特征、个体差异、任务条件的调节。未来可进一步探索注意对杏仁核情绪效价特异性的调节作用,探究动态情绪刺激加工时杏仁核的活动特点,考察心理障碍患者加工负性情绪时的杏仁核激活模式,并确定杏仁核的效价特异性在思维、计划、决策等高级认知过程中的表现。     

Regulation of brain activity in the fusiform face and parahippocampal place areas in 7–11-year-old children

Developmental studies have demonstrated that cognitive processes such as attention, suppression of interference and memory develop throughout childhood and adolescence. However, little is currently known about the development of top-down control mechanisms and their influence on cognitive performance. In the present study, we used functional magnetic resonance imaging to investigate modulation of activity in the ventral visual cortex in healthy 7–11-year-old children and young adults. The participants performed tasks that required attention to either face (Fs task) or scene (Sf task) images while trying to ignore distracting scene or face images, respectively. A face-selective area in the fusiform gyrus (fusiform face area, FFA) and an area responding preferentially to scene images in the parahippocampal gyrus (parahippocampal place area, PPA) were defined using functional localizers. Children responded slower and less accurately in the tasks than adults. In children, the right FFA was less selective to face images and regulation of activity between the Fs and Sf tasks was weaker compared to adults. In the PPA, selectivity to scenes and regulation of activity, there according to the task demands were comparable between children and adults. During the tasks, children activated prefrontal cortical areas including the middle (MFG) and superior (SFG) frontal gyrus more than adults. Functional connectivity between the right FFA and left MFG was stronger in adults than children in the Fs task. Children, on the other hand, had stronger functional connectivity than adults in the Sf task between the right FFA and right PPA and between right MFG and medial SFG. There were no group differences in the functional connectivity between the PPA and the prefrontal cortex (PFC). Together the results suggest that, in 7–11-year-old children, the FFA is still immature, whereas the selectivity to scenes and regulation of activity in the PPA is comparable to adults. The results also indicated functional immaturity of the PFC in children compared to adults and weaker connectivity between the PFC and the rFFA, explaining the weaker regulation of activity in the rFFA between the Fs and Sf tasks.     

睡眠剥夺影响恐惧情绪加工的认知神经机制

睡眠剥夺与恐惧情绪加工的各个过程息息相关。睡眠剥夺损害了恐惧的习得过程, 而且影响着杏仁核、内侧前额叶的活动及它们之间的功能连接; 睡眠剥夺削弱了恐惧记忆的巩固和再巩固过程, 不仅破坏了恐惧记忆再巩固过程相关蛋白质和酶的合成, 同时也影响着海马、杏仁核、内侧前额叶的活动以及它们之间的功能连接; 睡眠剥夺损害了恐惧的消退, 同时也改变了海马、杏仁核等相关脑区的活动模式。未来的研究应从睡眠剥夺影响恐惧情绪加工的认知神经机制、睡眠剥夺与恐惧情绪相关障碍的关系等角度展开, 力图深入理解睡眠剥夺影响恐惧情绪加工的认知神经机制。     

杏仁核对感觉刺激的情绪性加工:自动化过程和注意调控过程的整合

利用有限的认知资源应对多变的环境刺激,选择性注意和情绪加工一个重要的共同机制是优先化关键信息的加工。尽管情绪性刺激(特别是威胁刺激)能够影响注意资源的分配,但一些关键脑区(如杏仁核)的对情绪性刺激的加工是自动化过程还是受到注意调节一直是个有争议的问题。最新的结合高时间分辨率和高空间分辨率的神经生理记录研究表明,情绪加工的重要核团,杏仁核,对情绪性刺激的加工包含早期快速的不依赖于注意资源和认知加工负荷的自动化加工成分和晚期受到额-顶叶皮层自上而下的注意调控成分,这种功能整合证实杏仁核情绪性加工存在并行的皮层下和皮层通路。     

Altered Cortico-Limbic Functional Connectivity During an Empathy Task in Subjects with Post-Traumatic Stress Disorder

Empathy is a multidimensional construct consisting of cognitive (inferring mental states) and emotional (empathic concern) components. Emotional empathy is severely impaired in individuals affected by Post-Traumatic Stress Disorder (PTSD). Here, we investigated the neural correlates of such an emotional empathy dysfunction to shed light on the neural circuitry responsible for the social and emotional dysfunction in PTSD. We asked a group of PTSD and a group of healthy controls to solve a Multifaceted Empathy Test, measuring both cognitive and emotional empathy, and investigated the functional connectivity of the cortical areas involved in solving the test. The results revealed that, in healthy individuals, increased neural activity in the frontal cortex modulates activity in the insula while subjects perform the emotional empathy task; whereas, in individuals affected by PTSD, increased activity in limbic regions such the insula and the amygdala modulates activity in the frontal cortex while performing the emotional empathy task. These findings suggest that the lack of cortical top-down control of the frontal cortex on the limbic system in PTSD during empathic processing may explain the emotional and social difficulties experienced by individuals suffering from PTSD.     

Stress sensitive healthy females show less left amygdala activation in response to withdrawal-related visual stimuli under passive viewing conditions

The amygdalae are key players in the processing of a variety of emotional stimuli. Especially aversive visual stimuli have been reported to attract attention and activate the amygdalae. However, as it has been argued that passively viewing withdrawal-related images could attenuate instead of activate amygdalae neuronal responses, its role under passive viewing conditions remains unclear. Furthermore, because individual sensitivity to stress reactions has been shown to modulate amygdalae processing, the aim of the current event-related fMRI study was to investigate whether individual differences in stress proneness could influence amygdala responses while passively viewing withdrawal and approach-related visual images. We presented 14 healthy female subjects with a random sequence of images of happy 'healthy' baby faces (approach-related) and baby faces disfigured by severe dermatological conditions (withdrawal-related). No instructions were given other than to watch the images attentively. We integrated individual perceived stress (PSS) scores in our analysis. The processing of withdrawal-related pictures resulted in less left amygdala activity in females scoring higher on perceived stress. Our findings suggest that stress-sensitive healthy females are less able to fully attend to withdrawal-related visual material and in essence avoid exposure to such images in an effort to reduce strong psychophysiological responses. Although the relatively small number of participants limits drawing firm conclusions, we suggest that in passive viewing emotional brain imaging paradigms, individual information on stress proneness should be included in the interpretation of amygdala neuronal processes.     

Resisting emotional interference: Brain regions facilitating working memory performance during negative distraction

Survival-relevant information has privileged access to our awareness even during active cognitive engagement. Previous work has demonstrated that during working memory (WM) negative emotional distraction disrupts activation in the lateral prefrontal regions while also engaging the amygdala. Here, using slow eventrelated fMRI, we replicate and extend previous work examining the effect of negative emotional distraction on WM: (1) We demonstrate that prefrontal regions showed activation differences between correct and incorrect trials during negative, but not neutral, distraction. Specifically, frontopolar prefrontal cortex showed more deactivation for incorrect trials faced with negative distraction, whereas ventrolateral prefrontal regions showed less activation; (2) individual differences in amygdala activity predicted WM performance during negative as well as neutral distraction, such that lower activity predicted better performance; and (3) amygdala showed negative correlations with prefrontal and parietal cortical regions during resting state. However, during negative distraction, amygdala signals were more negatively correlated with prefrontal cortical regions than was found for resting state and neutral distraction. These results provide further evidence for an inverse relationship between dorsal prefrontal cortical regions and the amygdala when processing aversive stimuli competes with ongoing cognitive operations, and further support the importance of the prefrontal cortex in resisting emotional interference. Supplemental materials associated with this article may be downloaded from http://cabn.psychonomic-journals .org/content/supplemental.     

Cognitive and neural mechanisms of emotional memory

A highly adaptive aspect of human memory is the enhancement of explicit, consciously accessible memory for emotional stimuli. Recent findings from neuroimaging, neuropsychological, drug and neural stimulation studies indicate that emotional stimuli engage specific cognitive and neural mechanisms that enhance explicit memory. Emotional arousal influences memory via factors that act during memory encoding (attention and elaboration) and factors that modulate memory consolidation. Across studies, the amygdala has been consistently implicated as playing a key role in enhancing explicit memory for both pleasant and unpleasant emotional stimuli through modulation of encoding and consolidation processes.     

Cognitive and Emotional Abnormalities in Systemic Lupus Erythematosus: Evidence for Amygdala Dysfunction

Systemic lupus erythematosus (SLE) is a multi-system autoimmune disorder characterized by the production of autoantibodies. Approximately 30-50?% of patients produce autoantibodies directed against N-Methyl-D-aspartic acid receptors (NMDARs). Once they have gained access to brain tissue, these autoantibodies bind to the NR2A subunit of the NMDARs and synergize with glutamate to cause excitatory, non-inflammatory cell death or alter neuron function. Both humans with SLE and animal models of SLE have shown structural and functional damage to the amygdala. The amygdala is a brain region important for processing the emotional relevance of stimuli in the environment. It also serves to modulate perception, attention, and memory to facilitate the processing and learning of relevant stimuli. Research has linked amygdala damage to deficits in emotional memory and emotional behavior. Individuals with SLE often exhibit emotional dysregulation, such as lability and depression; however, the behavioral impact of possible amygdala dysfunction has yet to be studied in this population. The purpose of this review is to 1) examine possible associations between SLE, anti-NMDAR antibodies, amygdala damage, and emotional processing deficits and 2) to identify the clinical, social, and treatment implications for individuals with SLE who suffer from deficits in emotional processing.     

无关工作记忆表征的负性情绪信息能否捕获视觉注意?一项眼动研究

研究通过分析视觉搜索任务的首次注视点和行为反应时, 探讨无关工作记忆表征的负性情绪信息对视觉注意选择的影响。实验1发现在反映早期注意选择的首次注视点百分率指标上, 不管工作记忆表征的情绪效价如何, 均出现了显著的注意捕获效应; 实验2发现当采用中性情绪靶子刺激时, 首次注视点百分率指标上仍表现出了稳健的注意捕获效应; 在首次注视点持续时间指标上, 实验1和实验2均发现记忆匹配条件的干扰刺激显著小于控制条件的干扰刺激, 表现出注意的快速脱离; 而在行为反应时指标上, 早期的注意捕获效应消失(实验1), 甚至被反转为注意抑制效应(实验2)。这些结果表明在早期注意选择阶段, 记忆驱动的注意捕获效应不受工作记忆表征情绪效价的影响, 但认知控制会在早期注意捕获之后促使注意快速脱离记忆匹配的干扰刺激, 其作用效果受靶子刺激情绪效价的调节。     

Working memory load reduces the late positive potential and this effect is attenuated with increasing anxiety

Emotion regulation decreases the processing of arousing stimuli, as indexed by the late positive potential (LPP), an electrocortical component that varies in amplitude with emotional arousal. Emotion regulation increases activity in the prefrontal areas associated with cognitive control, including the dosolateral prefrontal cortex (DLPFC). The present study manipulated working memory load, known to activate the DLPFC, and recorded the LPP elicited by aversive and neutral IAPS pictures presented during the retention interval. The LPP was larger on low-load compared to high-load trials, and on trials with aversive compared to neutral pictures. These LPP data suggest that emotional content and working memory load have opposing effects on attention to distracting stimuli. State anxiety was associated with reduced modulation of the LPP by working memory load. Results are discussed in terms of competition for attention between emotion and cognition and suggest a relationship between DLPFC activation and the allocation of attentional resources to distracting visual stimuli–a relationship that may be disrupted with increasing anxiety.     

Emotional stimuli exert parallel effects on attention and memory

Because emotional and neutral stimuli typically differ on non-emotional dimensions, it has been difficult to determine conclusively which factors underlie the ability of emotional stimuli to enhance immediate long-term memory. Here we induced arousal by varying participants' goals, a method that removes many potential confounds between emotional and non-emotional items. Hungry and sated participants encoded food and clothing images under divided attention conditions. Sated participants attended to and recalled food and clothing images equivalently. Hungry participants performed worse on the concurrent tone-discrimination task when they viewed food relative to clothing images, suggesting enhanced attention to food images, and they recalled more food than clothing images. A follow-up regression analysis of the factors predicting memory for individual pictures revealed that food images had parallel effects on attention and memory in hungry participants, so that enhanced attention to food images did not predict their enhanced memory. We suggest that immediate long-term memory for food is enhanced in the hungry state because hunger leads to more distinctive processing of food images rendering them more accessible during retrieval.     

催产素影响恐惧习得和消退的认知神经机制

恐惧是一种基本的情绪, 在人类的生存和适应中发挥着重要作用。先前的研究表明, 杏仁核、背侧前扣带回、脑岛等脑区是条件化恐惧习得的认知神经基础, 杏仁核、海马和腹内侧前额叶等脑区在恐惧消退过程中发挥重要作用。研究发现, 催产素与恐惧习得和恐惧消退过程密切相关。恐惧习得过程中, 催产素影响杏仁核、背侧前扣带回的活动, 影响杏仁核与背侧前扣带回和脑干间的功能连接, 促进或抑制恐惧习得过程; 恐惧消退过程中, 催产素影响了杏仁核和腹内侧前额叶的活动, 并且影响杏仁核与内侧前额叶和海马间的功能连接, 促进或抑制恐惧消退过程。未来研究应从性别差异、神经网络模型、身心发育和病理研究等角度展开, 力图深入理解催产素影响恐惧情绪加工的认知神经机制。     

睡眠对恐惧学习的影响及其认知神经机制

睡眠问题可能会诱发恐惧相关情绪障碍(焦虑、创伤性应激障碍、恐怖症等),研究睡眠影响恐惧学习的认知神经机制,有助于增强对恐惧相关情绪障碍的预测、诊断和治疗。以往研究表明睡眠剥夺影响恐惧习得和消退主要是通过抑制vmPFC活动,阻碍其与杏仁核的功能连接,从而导致恐惧习得增强或是消退学习受损。进一步研究发现睡眠不同阶段对恐惧学习相关脑区有独特的影响:剥夺(缺乏)快速眼动睡眠会抑制vmPFC活动、增强杏仁核、海马激活,导致恐惧习得增强,消退学习受损,此外边缘皮层的功能连接减少破坏了记忆巩固(恐惧记忆和消退记忆);而慢波睡眠主要与海马变化有关,慢波睡眠期间进行目标记忆重激活可促进恐惧消退学习。未来研究需要增加睡眠影响恐惧泛化的神经机制研究、及昼夜节律中断对恐惧消退的影响,以及关注动物睡眠研究向人类睡眠研究转化中存在的问题。     

Functional connectivity differences in autism during face and car recognition: underconnectivity and atypical age‐related changes

Face recognition abilities improve between adolescence and adulthood over typical development (TD), but plateau in autism, leading to increasing face recognition deficits in autism later in life. Developmental differences between autism and TD may reflect changes between neural systems involved in the development of face encoding and recognition. Here, we focused on whole‐brain connectivity with the fusiform face area (FFA), a well‐established face‐preferential brain region. Older children, adolescents, and adults with and without autism completed the Cambridge Face Memory Test, and a matched car memory test, during fMRI scanning. We then examined task‐based functional connectivity between the FFA and the rest of the brain, comparing autism and TD groups during encoding and recognition of face and car stimuli. The autism group exhibited underconnectivity, relative to the TD group, between the FFA and frontal and primary visual cortices, independent of age. Underconnectivity with the medial and rostral lateral prefrontal cortex was face‐specific during encoding and recognition, respectively. Conversely, underconnectivity with the L orbitofrontal cortex was evident for both face and car encoding. Atypical age‐related changes in connectivity emerged between the FFA and the R temporoparietal junction, and R dorsal striatum for face stimuli only. Similar differences in age‐related changes in autism emerged for FFA connectivity with the amygdala across both face and car recognition. Thus, underconnectivity and atypical development of functional connectivity may lead to a less optimal face‐processing network in the context of increasing general and social cognitive deficits in autism.