ARTICLE UPDATE - Functional connectivity of the human amygdala using resting state fMRI.

Roy AK, Shehzad Z, Margulies DS, Kelly AM, Uddin LQ, Gotimer K, Biswal BB, Castellanos FX, Milham MP.

Neuroimage, in press

The amygdala is composed of structurally and functionally distinct nuclei that contribute to the processing of emotion through interactions with other subcortical and cortical structures. While these circuits have been studied extensively in animals, human neuroimaging investigations of amygdala-based networks have typically considered the amygdala as a single structure, which likely masks contributions of individual amygdala subdivisions. The present study uses resting state functional magnetic resonance imaging (fMRI) to test whether distinct functional connectivity patterns, like those observed in animal studies, can be detected across three amygdala subdivisions: laterobasal, centromedial, and superficial. In a sample of 65 healthy adults, voxelwise regression analyses demonstrated positively-predicted ventral and negatively-predicted dorsal networks associated with the total amygdala, consistent with previous animal and human studies. Investigation of individual amygdala subdivisions revealed distinct differences in connectivity patterns within the amygdala and throughout the brain. Spontaneous activity in the laterobasal subdivision predicted activity in temporal and frontal regions, while activity in the centromedial nuclei predicted activity primarily in striatum. Activity in the superficial subdivision positively predicted activity throughout the limbic lobe. These findings suggest that resting state fMRI can be used to investigate human amygdala networks at a greater level of detail than previously appreciated, allowing for the further advancement of translational models.

ARTICLE UPDATE - Behavioral triggers of skin conductance responses and their neural correlates in the primate amygdala.

Laine CM, Spitler KM, Mosher CP, Gothard KM.

Journal of Neurophysiology, in press

The amygdala plays a crucial role in evaluating the emotional significance of stimuli and in transforming the results of this evaluation into appropriate autonomic responses. Lesion and stimulation studies suggest involvement of the amygdala in the generation of the skin conductance response (SCR), which is an indirect measure of autonomic activity that has been associated with both emotion and attention. It is unclear if this involvement marks an emotional reaction to an external stimulus, or sympathetic arousal regardless of its origin. We recorded skin conductance in parallel with single unit activity from the right amygdala of two rhesus monkeys during a rewarded image viewing task, and while the monkeys sat alone in a dimly lit room, drifting in and out of sleep. In both experimental conditions, we found similar SCR-related modulation of activity at the single unit and population level. This suggests that the amygdala contributes to the production or modulation of SCRs regardless of the source of sympathetic arousal.

ARTICLE UPDATE - Emotion, decision making, and the amygdala.

Seymour B, Dolan R.

Neuron, 58, 662-671

Emotion plays a critical role in many contemporary accounts of decision making, but exactly what underlies its influence and how this is mediated in the brain remain far from clear. Here, we review behavioral studies that suggest that Pavlovian processes can exert an important influence over choice and may account for many effects that have traditionally been attributed to emotion. We illustrate how recent experiments cast light on the underlying structure of Pavlovian control and argue that generally this influence makes good computational sense. Corresponding neuroscientific data from both animals and humans implicate a central role for the amygdala through interactions with other brain areas. This yields a neurobiological account of emotion in which it may operate, often covertly, to optimize rather than corrupt economic choice.

ARTICLE UPDATE - Amygdala contribution to selective dimensions of emotion.

Berntson GG, Bechara A, Damasio H, Tranel D, Cacioppo JT.

Social, Cognitive and Affective Neuroscience, 2, 123-129

The amygdala has been implicated in emotional processes, although the precise nature of the emotional deficits following amygdala lesions remains to be fully elucidated. Cognitive disturbances in the perception, recognition or memory of emotional stimuli have been suggested by some, whereas others have proposed changes in emotional arousal. To address this issue, measures of emotional arousal and valence (positivity and negativity) to a graded series of emotional pictures were obtained from patients with lesions of the amygdala and from a clinical contrast group with lesions that spared this structure. Relative to the contrast group, patients with damage to the amygdala evidenced a complete lack of an arousal gradient across negative stimuli, although they displayed a typical arousal gradient to positive stimuli. These results were not attributable to the inability of amygdala patients to process the hostile or hospitable nature of the stimuli, as the amygdala group accurately recognized and categorized both positive and negative features of the stimuli. The relative lack of emotional arousal to negative stimuli may account for many of the clinical features of amygdala lesions.

ARTICLE UPDATE - The amygdala and the experience of affect.

Barrett LF, Bliss-Moreau E, Duncan SL, Rauch SL, Wright CI.

Social Cognitive Affective Neuroscience, 2, 73-83

The current study examined the hypothesis that amygdala activation serves as a neural precondition for negative affective experience. Participants' affective experience was measured by asking them to report on their momentary experiences several times a day over the course of a month using an electronic experience-sampling procedure. One year later, participants viewed backwardly masked depictions of fear while functional magnetic resonance imaging was used to measure their amygdala and fusiform gyrus activation. Negative affect, as measured during the experience-sampling procedure 1-year prior, was positively correlated with amygdala activation in response to these brief presentations of fear depictions. Furthermore, descriptive analyses indicated that fusiform gyrus activation and negative affective experience in the scanner were associated for participants reporting increased nervousness during the imaging procedure. The results are consistent with the interpretation that the amygdala contributes to negative affective experience by increasing perceptual sensitivity for negative stimuli.

ARTICLE UPDATE - Working Memory for Social Cues Recruits Orbitofrontal Cortex and Amygdala: A Functional Magnetic Resonance Imaging Study of Delayed M

Lopresti ML, Schon K, Tricarico MD, Swisher JD, Celone KA, Stern CE.

The Journal of Neuroscience, 28, 3718-3728.

During everyday interactions, we continuously monitor and maintain information about different individuals and their changing emotions in memory. Yet to date, working memory (WM) studies have primarily focused on mechanisms for maintaining face identity, but not emotional expression, and studies investigating the neural basis of emotion have focused on transient activity, not delay related activity. The goal of this functional magnetic resonance imaging study was to investigate WM for two critical social cues: identity and emotion. Subjects performed a delayed match-to-sample task that required them to match either the emotional expression or the identity of a face after a 10 s delay. Neuroanatomically, our predictions focused on the orbitofrontal cortex (OFC) and the amygdala, as these regions have previously been implicated in emotional processing and long-term memory, and studies have demonstrated sustained OFC and medial temporal lobe activity during visual WM. Consistent with previous studies, transient activity during the sample period representing emotion and identity was found in the superior temporal sulcus and inferior occipital cortex, respectively. Sustained delay-period activity was evident in OFC, amygdala, and hippocampus, for both emotion and identity trials. These results suggest that, although initial processing of emotion and identity is accomplished in anatomically segregated temporal and occipital regions, sustained delay related memory for these two critical features is held by the OFC, amygdala and hippocampus. These regions share rich connections, and have been shown previously to be necessary for binding features together in long-term memory. Our results suggest a role for these regions in active maintenance as well.

ARTICLE UPDATE - Learning affective values for faces is expressed in amygdala and fusiform gyrus

Predrag Petrovic, Raffael Kalisch, Mathias Pessiglione, Tania Singer and Raymond J. Dolan

Social Cognitive and Affective Neuroscience, in press

To monitor the environment for social threat humans must build affective evaluations of others. These evaluations are malleable and to a high degree shaped by responses engendered by specific social encounters. The precise neuronal mechanism by which these evaluations are constructed is poorly understood. We tested a hypothesis that conjoint activity in amygdala and fusiform gyrus would correlate with acquisition of social stimulus value. We tested this using a reinforcement learning algorithm, Q-learning, that assigned values to faces as a function of a history of pairing, or not pairing, with aversive shocks. Behaviourally, we observed a correlation between conditioning induced changes in skin conductance response (SCR) and subjective ratings for likeability of faces. Activity in both amygdala and fusiform gyrus (FG) correlated with the output of the reinforcement learning algorithm parameterized by these ratings. In amygdala, this effect was greater for averted than direct gaze faces. Furthermore, learning-related activity change in these regions correlated with SCR and subjective ratings. We conclude that amygdala and fusiform encode affective value in a manner that closely approximates a standard computational solution to learning.

ARTICLE UPDATE - Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies.

Costafreda SG, Brammer MJ, David AS, Fu CH.

Brain Research Review, in press (Note that this link will direct you to download this article in pdf format. So it might not work for everyone)

Although amygdala activity has been purported to be modulated by affective and non-affective factors, considerable controversy remains on its precise functional nature. We conducted a meta-analysis of 385 functional neuroimaging studies of emotional processing, examining the effects of experimental characteristics on the probability of detecting amygdala activity. All emotional stimuli were associated with higher probability of amygdala activity than neutral stimuli. Comparable effects were observed for most negative and positive emotions, however there was a higher probability of activation for fear and disgust relative to happiness. The level of attentional processing affected amygdala activity, as passive processing was associated with a higher probability of activation than active task instructions. Gustatory-olfactory and visual stimulus modalities increased the probability of activation relative to internal stimuli. Aversive learning increased the probability of amygdala activation as well. There was some evidence of hemispheric specialization with a relative left-lateralization for stimuli containing language and a relative right-lateralization for masked stimuli. Methodological variables, such as type of analysis and magnet strength, were also independent predictors of amygdala activation.

ARTICLE UPDATE - Neural mechanisms mediating optimism bias

Tali Sharot, Alison M. Riccardi, Candace M. Raio & Elizabeth A. Phelps

Nature, 450, 102-105

Humans expect positive events in the future even when there is no evidence to support such expectations. For example, people expect to live longer and be healthier than average, they underestimate their likelihood of getting a divorce, and overestimate their prospects for success on the job market. We examined how the brain generates this pervasive optimism bias. Here we report that this tendency was related specifically to enhanced activation in the amygdala and in the rostral anterior cingulate cortex when imagining positive future events relative to negative ones, suggesting a key role for areas involved in monitoring emotional salience in mediating the optimism bias. These are the same regions that show irregularities in depression, which has been related to pessimism. Across individuals, activity in the rostral anterior cingulate cortex was correlated with trait optimism. The current study highlights how the brain may generate the tendency to engage in the projection of positive future events, suggesting that the effective integration and regulation of emotional and autobiographical information supports the projection of positive future events in healthy individuals, and is related to optimism.

ARTICLE UPDATE - The human emotional brain without sleep - a prefrontal amygdala disconnect.

Yoo SS, Gujar N, Hu P, Jolesz FA, Walker MP.

Current Biology, 17, R877-878

Sleep deprivation is known to impair a range of functions, including immune regulation and metabolic control, as well as neurocognitive processes, such as learning and memory [1]. But evidence for the role of sleep in regulating our emotional brain-state is surprisingly scarce, and while the dysregulation of affective stability following sleep loss has received subjective documentation [2,3], any neural examination remains absent. Clinical evidence suggests that sleep and emotion interact; nearly all psychiatric and neurological disorders expressing sleep disruption display corresponding symptoms of affective imbalance [4]. Independent of sleep, knowledge of the basic neural and cognitive mechanisms regulating emotion is remarkably advanced. The amygdala has a well-documented role in the processing of emotionally salient information, particularly aversive stimuli [5,6]. The extent of amygdala engagement can also be influenced by a variety of connected systems, particularly the medial-prefrontal cortex (MPFC); the MPFC is proposed to exert an inhibitory, top-down control of amygdala function, resulting in contextually appropriate emotional responses [5,6]. We have focused on this network and using functional magnetic resonance image (fMRI) have obtained evidence, reported here, that a lack of sleep inappropriately modulates the human emotional brain response to negative aversive stimuli (see Supplemental data available on-line with this issue).

ARTICLE UPDATE - The role of medial temporal lobe in item recognition and source recollection of emotional stimuli

Dougal, Sonya; Phelps, Elizabeth A.; Davachi, Lila

Cognitive, Affective, & Behavioral Neuroscience, 7, 233-242

Recent neuroimaging results suggest that distinct regions within the medial temporal lobe (MTL) may differentially support the episodic encoding of item and relational information for nonemotional stimuli (for a review, see Davachi, 2006). The present study was designed to assess whether these findings generalize to emotional stimuli. Behaviorally, we found that emotion reduced item recognition accuracy but did not reliably affect relational memory. fMRI analyses revealed that neutral and emotional words elicited distinct activation patterns within MTL regions predictive of subsequent memory. Consistent with previous findings for neutral words, hippocampal activation predicted later relational memory, whereas activation in the perirhinal cortex predicted successful item recognition. However, for emotional words, activation in the amygdala, hippocampus, and posterior parahippocampal cortex predicted item recognition only. These data suggest that MTL regions differentially support encoding of neutral and emotional stimuli.

ARTICLE UPDATE - Unilateral Amygdala Lesions Hamper Attentional Orienting Triggered by Gaze Direction

Tomoko Akiyama, Motoichiro Kato, Taro Muramatsu, Satoshi Umeda, Fumie Saito and Haruo Kashima

Cerebral Cortex, in press

The newly discovered deficit in a bilateral amygdala-damaged case, of not being able to allocate attention to the critical feature of a face (Adolphs R, Gosselin F, Buchanan TW, Tranel D, Schyns P, Damasio AR. 2005. A mechanism for impaired fear recognition after amygdala damage. Nature. 433:68--72.), has opened a new window into the function of the amygdala. This case implies that the amygdala might be essential in detecting potentially relevant social stimuli, and directing attention accordingly. In this study, we have sought to test this implication by investigating the behavioral performance of 5 unilateral amygdala-damaged subjects on spatial cueing tasks. The tasks employed central gaze and arrow direction as cues to trigger attentional orienting in peripheral target detection. Although age-matched normal controls demonstrated a significant congruency effect such that targets presented congruently to cue direction elicited faster detection, amygdala subjects demonstrated no such congruency effect for gaze cues in the face of a significant congruency effect for arrow cues. The results suggest that the social valence of a stimulus is critical for amygdala involvement in visual processing. The results also support the implicated role of the amygdala in detecting and analyzing relevant social stimuli, and orienting attention accordingly.

ARTICLE UPDATE - Social learning of fear

Andreas Olsson & Elizabeth A Phelps

Nature Neuroscience, 10, 1095-1102

Research across species highlights the critical role of the amygdala in fear conditioning. However, fear conditioning, involving direct aversive experience, is only one means by which fears can be acquired. Exploiting aversive experiences of other individuals through social fear learning is less risky. Behavioral research provides important insights into the workings of social fear learning, and the neural mechanisms are beginning to be understood. We review research suggesting that an amygdala-centered model of fear conditioning can help to explain social learning of fear through observation and instruction. We also describe how observational and instructed fear is distinguished by involvement of additional neural systems implicated in social-emotional behavior, language and explicit memory, and propose a modified conditioning model to account for social fear learning. A better understanding of social fear learning promotes integration of biological principles of learning with cultural evolution.

ARTICLE UPDATE - Threat sensitivity as assessed by automatic amygdala response to fearful faces predicts speed of visual search for facial expression.

Ohrmann P, Rauch AV, Bauer J, Kugel H, Arolt V, Heindel W, Suslow T.

Experimental Brain Research, in press

It has been argued that the amygdala represents an integral component of a vigilance system that is primarily involved in the perception of ambiguous stimuli of biological relevance. The present investigation was conducted to examine the relationship between automatic amygdala responsivity to fearful faces which may be interpreted as an index of trait-like threat sensitivity and spatial processing characteristics of facial emotions. During 3T fMRI scanning, pictures of human faces bearing fearful, angry, and happy expressions were presented to 20 healthy volunteers using a backward masking procedure based on neutral facial expressions. Subsequently, a computer-based face-in-the-crowd task using schematic face stimuli was administered. The neural response of the (right) amygdala to masked fearful faces correlated consistently with response speed to negative and neutral faces. Neither amygdala activation during the masked presentation of angry faces nor amygdala activation during the presentation of happy faces was correlated with any of the response latencies in the face-in-the-crowd task. Our results suggest that amygdala responsivity to masked facial expression is differentially related to the general visual search speed for facial expression. Neurobiologically defined threat sensitivity seems to represent an important determinant of visual scanning behaviour.

ARTICLE UPDATE - Visual presentation of phobic stimuli: Amygdala activation via an extrageniculostriate pathway?

Liesbet Goossens, Koen Schruers, Ronald Peeters, Eric Griez and Stefan Sunaert

Psychiatry Research: Neuroimaging, in press

In the present study, event-related functional magnetic resonance imaging (fMRI) was used to examine the neural correlates of phobic fear by exposing spider phobic subjects to a visual presentation of spiders. In contrast to control subjects, spider phobics showed significantly increased activation in the amygdala and the pulvinar nucleus of the thalamus on the basis of region of interest (ROI) analysis. Furthermore, voxelwise analysis revealed increased activation related to phobia-specific pictures bilaterally in the anterior cingulate cortex, the left insular cortex and bilaterally in the supplementary motor area. These findings confirm the involvement of the amygdala in the processing of phobia-relevant stimuli as found earlier in a recent study. Moreover, the thalamus findings support the involvement of an extrageniculostriate pathway in the process of phobic fear.

ARTICLE UPDATE - Feeling the Real World: Limbic Response to Music Depends on Related Content

Eran Eldar, Ori Ganor, Roee Admon, Avraham Bleich and Talma Hendler

Cerebral Cortex, in press

Emotions are often object related—they are about someone or something in the world. It is yet an open question whether emotions and the associated perceptual contents that they refer to are processed by different parts of the brain or whether the brain regions that mediate emotions are also involved in the processing of the associated content they refer to. Using functional magnetic resonance imaging, we showed that simply combining music (rich in emotion but poor in information about the concrete world) with neutral films (poor in emotionality but rich in real-world details) yields increased activity in the amygdala, hippocampus, and lateral prefrontal regions. In contrast, emotional music on its own did not elicit a differential response in these regions. The finding that the amygdala, the heart of the emotional brain, responds increasingly to an emotional stimulus when it is associated with realistic scenes supports a fundamental role for concrete real-world content in emotional processing.

ARTICLE UPDATE - The role of the amygdala in visual awareness.

Duncan S, Barrett LF.

Trends in Cognitive Sciences, in press

Pessoa and colleagues recently reported the novel finding that objective awareness of a negative stimulus is associated with coactivation of the amygdala and fusiform gyrus. Based on the neuroanatomical connections of the amygdala, we suggest that the amygdala is acting to increase neural activity in the fusiform gyrus, thereby increasing the likelihood that visual representations that have affective value reach awareness. The psychological consequence is that a person's momentary affective state might help to select the contents of conscious experience.

ARTICLE UPDATE - Learning fears by observing others: the neural systems of social fear transmission

Andreas Olsson, Katherine I. Nearing and Elizabeth A. Phelps

Social Cognitive and Affective Neuroscience, in press

Classical fear conditioning has been used as a model paradigm to explain fear learning across species. In this paradigm, the amygdala is known to play a critical role. However, classical fear conditioning requires first-hand experience with an aversive event, which may not be how most fears are acquired in humans. It remains to be determined whether the conditioning model can be extended to indirect forms of learning more common in humans. Here we show that fear acquired indirectly through social observation, with no personal experience of the aversive event, engages similar neural mechanisms as fear conditioning. The amygdala was recruited both when subjects observed someone else being submitted to an aversive event, knowing that the same treatment awaited themselves, and when subjects were subsequently placed in an analogous situation. These findings confirm the central role of the amygdala in the acquisition and expression of observational fear learning, and validate the extension of cross-species models of fear conditioning to learning in a human sociocultural context. Our findings also provides new insights into the relationship between learning from, and empathizing with, fearful others. This study suggests that indirectly attained fears may be as powerful as fears originating from direct experiences.