ARTICLE UPDATE - Unconscious fear influences emotional awareness of faces and voices

B. de Gelder, J. S. Morris and R. J. Dolan

PNAS, 102, 18682-18687

Nonconscious recognition of facial expressions opens an intriguing possibility that two emotions can be present together in one brain with unconsciously and consciously perceived inputs interacting. We investigated this interaction in three experiments by using a hemianope patient with residual nonconscious vision. During simultaneous presentation of facial expressions to the intact and the blind field, we measured interactions between conscious and nonconsciously recognized images. Fear-specific congruence effects were expressed as enhanced neuronal activity in fusiform gyrus, amygdala, and pulvinar. Nonconscious facial expressions also influenced processing of consciously recognized emotional voices. Emotional congruency between visual and an auditory input enhances activity in amygdala and superior colliculus for blind, relative to intact, field presentation of faces. Our findings indicate that recognition of fear is mandatory and independent of awareness. Most importantly, unconscious fear recognition remains robust even in the light of a concurrent incongruent happy facial expression or an emotional voice of which the observer is aware.

ARTICLE UPDATE - Neural mechanism for judging the appropriateness of facial affect

Ji-Woong Kim, Jae-Jin Kim, Bum Seok Jeong, Seon Wan Ki, Dong-Mi Im, Soo Jung Lee and Hong Shick Lee

Cognitive Brain Research, 25, 659-667

Questions regarding the appropriateness of facial expressions in particular situations arise ubiquitously in everyday social interactions. To determine the appropriateness of facial affect, first of all, we should represent our own or the other's emotional state as induced by the social situation. Then, based on these representations, we should infer the possible affective response of the other person. In this study, we identified the brain mechanism mediating special types of social evaluative judgments of facial affect in which the internal reference is related to theory of mind (ToM) processing. Many previous ToM studies have used non-emotional stimuli, but, because so much valuable social information is conveyed through nonverbal emotional channels, this investigation used emotionally salient visual materials to tap ToM. Fourteen right-handed healthy subjects volunteered for our study. We used functional magnetic resonance imaging to examine brain activation during the judgmental task for the appropriateness of facial affects as opposed to gender matching tasks. We identified activation of a brain network, which includes both medial frontal cortex, left temporal pole, left inferior frontal gyrus, and left thalamus during the judgmental task for appropriateness of facial affect compared to the gender matching task. The results of this study suggest that the brain system involved in ToM plays a key role in judging the appropriateness of facial affect in an emotionally laden situation. In addition, our result supports that common neural substrates are involved in performing diverse kinds of ToM tasks irrespective of perceptual modalities and the emotional salience of test materials.

ARTICLE UPDATE - Doing the right thing: A common neural circuit for appropriate violent or compassionate behavior

John A. King, R. James R. Blair, Derek G.V. Mitchell, Raymond J. Dolan and Neil Burgess

NeuroImage, in press

Humans have a considerable facility to adapt their behavior in a manner that is appropriate to social or societal context. A failure of this ability can lead to social exclusion and is a feature of disorders such as psychopathy and disruptive behavior disorder. We investigated the neural basis of this ability using a customized video game played by 12 healthy participants in an fMRI scanner. Two conditions involved extreme examples of context-appropriate action: shooting an aggressive humanoid assailant or healing a passive wounded person. Two control conditions involved carefully matched stimuli paired with inappropriate actions: shooting the person or healing the assailant. Surprisingly, the same circuit, including the amygdala and ventromedial prefrontal cortex, was activated when participants acted in a context-appropriate manner, whether being compassionate towards an injured conspecific or aggressive towards a violent assailant. The findings indicate a common system that guides behavioral expression appropriate to social or societal context irrespective of its aggressive or compassionate nature.

ARTICLE UPDATE - How brains beware: neural mechanisms of emotional attention

Patrik Vuilleumier

Trends in Cognitive Sciences, in press

Emotional processes not only serve to record the value of sensory events, but also to elicit adaptive responses and modify perception. Recent research using functional brain imaging in human subjects has begun to reveal neural substrates by which sensory processing and attention can be modulated by the affective significance of stimuli. The amygdala plays a crucial role in providing both direct and indirect top-down signals on sensory pathways, which can influence the representation of emotional events, especially when related to threat. These modulatory effects implement specialized mechanisms of ‘emotional attention’ that might supplement but also compete with other sources of top-down control on perception. This work should help to elucidate the neural processes and temporal dynamics governing the integration of cognitive and affective influences in attention and behaviour.

ARTICLE UPDATE - Dissociable networks for the expectancy and perception of emotional stimuli in the human brain

Felix Bermpohl, Alvaro Pascual-Leone, Amir Amedi, Lotfi B. Merabet, Felipe Fregni, Nadine Gaab, David Alsop, Gottfried Schlaug and Georg Northoff

NeuroImage, in press

William James posited that comparable brain regions were implicated in the anticipation and perception of a stimulus; however, dissociable networks (at least in part) may also underlie these processes. Recent functional neuroimaging studies have addressed this issue by comparing brain systems associated with the expectancy and perception of visual, tactile, nociceptive, and reward stimuli. In the present fMRI study, we addressed this issue in the domain of pictorial emotional stimuli (IAPS). Our paradigm involved the experimental conditions emotional expectancy, neutral expectancy, emotional picture perception, and neutral picture perception. Specifically, the emotional expectancy cue was uncertain in that it did not provide additional information regarding the positive or negative valence of the subsequent picture. Neutral expectancy and neutral picture perception served as control conditions, allowing the identification of expectancy and perception effects specific for emotion processing. To avoid contamination of the perception conditions by the preceding expectancy periods, 50% of the pictorial stimuli were presented without preceding expectancy cues. We found that the emotional expectancy cue specifically produced activation in the supracallosal anterior cingulate, cingulate motor area, and parieto-occipital sulcus. These regions were not significantly activated by emotional picture perception which recruited a different neuronal network, including the amygdala, insula, medial and lateral prefrontal cortex, cerebellum, and occipitotemporal areas. This dissociation may reflect a distinction between anticipatory and perceptive components of emotional stimulus processing.

ARTICLE UPDATE - Changes in effective connectivity during incidental and intentional perception of fearful faces

G. de Marco, M. de Bonis, P. Vrignaud, M.C. Henry-Feugeas and I. Peretti

NeuroImage, in press

The present fMRI study examined effective connectivity within an emotional network composed of three brain areas: Amygdala (AMY), Anterior Cingulate Cortex (AAC) and Orbito-Frontal (OFC) in processing fearful faces. Two tasks: an incidental perception (gender identification) and an intentional detection (effortful discrimination) task were performed by 14 and 10 young healthy volunteers, respectively. Participants were scanned while viewing fearful, neutral and ambiguous facial expressions. Effective connectivity was assessed using Structural Equation Modeling (SEM). Results show that the hypothetical network fits the experimental data for both tasks and in both hemispheres. The comparison between Tasks 1 and 2 reveals significant differences in strength and direction of the connectivity patterns for the left and to a less stringent threshold for the right hemisphere. The path coefficients analysis suggests that the fearful information generated in AMY, reaches the OFC through the ACC in incidental perception, while in intentional perception, the route followed is in a reverse direction from OFC to ACC. Our findings confirm a differential brain connectivity between incidental and intentional processing of fearful faces.

ARTICLE UPDATE - “We All Look the Same to Me”: Positive Emotions Eliminate the Own-Race Bias in Face Recognition

Johnson, Kareem J., Fredrickson, Barbara L.

Psychological Science, 16, 875-881.

Extrapolating from the broaden-and-build theory, we hypothesized that positive emotion may reduce the own-race bias in facial recognition. In Experiments 1 and 2, Caucasian participants (N= 89) viewed Black and White faces for a recognition task. They viewed videos eliciting joy, fear, or neutrality before the learning (Experiment 1) or testing (Experiment 2) stages of the task. Results reliably supported the hypothesis. Relative to fear or a neutral state, joy experienced before either stage improved recognition of Black faces and significantly reduced the own-race bias. Discussion centers on possible mechanisms for this reduction of the own-race bias, including improvements in holistic processing and promotion of a common in-group identity due to positive emotions.

ARTICLE UPDATE - Attention modulates the processing of emotional expression triggered by foveal faces

Amanda Holmes, Monika Kiss and Martin Eimer

Neuroscience Letters, 394, 48-52.

To investigate whether the processing of emotional expression for faces presented within foveal vision is modulated by spatial attention, event-related potentials (ERPs) were recorded in response to stimulus arrays containing one fearful or neutral face at fixation, which was flanked by a pair of peripheral bilateral lines. When attention was focused on the central face, an enhanced positivity was elicited by fearful as compared to neutral faces. This effect started at 160 ms post-stimulus, and remained present for the remainder of the 700 ms analysis interval. When attention was directed away from the face towards the line pair, the initial phase of this emotional positivity remained present, but emotional expression effects beyond 220 ms post-stimulus were completely eliminated. These results demonstrate that when faces are presented foveally, the initial rapid stage of emotional expression processing is unaffected by attention. In contrast, attentional task instructions are effective in inhibiting later, more controlled stages of expression analysis.

ARTICLE UPDATE - Arousal and valence effects on event-related P3a and P3b during emotional categorization.

Delplanque S, Silvert L, Hot P, Rigoulot S, Sequeira H.

International Journal of Psychophysiology, in press

Due to the adaptive value of emotional situations, categorizing along the valence dimension may be supported by critical brain functions. The present study examined emotion-cognition relationships by focusing on the influence of an emotional categorization task on the cognitive processing induced by an oddball-like paradigm. Event-related potentials (ERPs) were recorded from subjects explicitly asked to categorize along the valence dimension (unpleasant, neutral or pleasant) deviant target pictures embedded in a train of standard stimuli. Late positivities evoked in response to the target pictures were decomposed into a P3a and a P3b and topographical differences were observed according to the valence content of the stimuli. P3a showed enhanced amplitudes at posterior sites in response to unpleasant pictures as compared to both neutral and pleasant pictures. This effect is interpreted as a negativity bias related to attentional processing. The P3b component was sensitive to the arousal value of the stimulation, with higher amplitudes at several posterior sites for both types of emotional pictures. Moreover, unpleasant pictures evoked smaller amplitudes than pleasant ones at fronto-central sites. Thus, the context updating process may be differentially modulated by the affective arousal and valence of the stimulus. The present study supports the assumption that, during an emotional categorization, the emotional content of the stimulus may modulate the reorientation of attention and the subsequent updating process in a specific way.

ARTICLE UPDATE - Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior

Phelps, E., & LeDoux, J.

Neuron, 48, 175-187

Research on the neural systems underlying emotion in animal models over the past two decades has implicated the amygdala in fear and other emotional processes. This work stimulated interest in pursuing the brain mechanisms of emotion in humans. Here, we review research on the role of the amygdala in emotional processes in both animal models and humans. The review is not exhaustive, but it highlights five major research topics that illustrate parallel roles for the amygdala in humans and other animals, including implicit emotional learning and memory, emotional modulation of memory, emotional influences on attention and perception, emotion and social behavior, and emotion inhibition and regulation.

ARTICLE UPDATE - Segregated neural representation of distinct emotion dimensions in the prefrontal cortex—an fMRI study

Simone Grimm, Conny F. Schmidt, Felix Bermpohl, Alexander Heinzel, Yuliya Dahlem, Michael Wyss, Daniel Hell, Peter Boesiger, Heinz Boeker and Georg Northoff

NeuroImage, in press

Emotions are frequently characterized by distinct dimensions such as valence, intensity, and recognition. However, the exact neural representation of these dimensions in different prefrontal cortical regions remains unclear. One of the problems in revealing prefrontal cortical representation is that the very same regions are also involved in cognitive functions associated with emotion processing. We therefore conducted an fMRI study involving the viewing of emotional pictures (using the International Affective Picture System; IAPS) and controlled for associated cognitive processing like judgment and preceding attention. Functional activation was correlated with subjective post-scanning ratings of valence, intensity, and recognition. Valence significantly correlated with the functional response in ventromedial prefrontal cortex (VMPFC) and dorsolateral prefrontal cortex (DLPFC), intensity with activation in ventrolateral prefrontal cortex (VLPFC) and dorsomedial prefrontal cortex (DMPFC), and recognition with the functional response in perigenual anterior cingulate cortex (PACC). In conclusion, our results indicate segregated neural representation of the different emotion dimensions in different prefrontal cortical regions.

ARTICLE UPDATE - Neural mechanism for judging the appropriateness of facial affect

Ji-Woong Kim, Jae-Jin Kim, Bum Seok Jeong, Seon Wan Ki, Dong-Mi Im, Soo Jung Lee and Hong Shick Lee

Cognitive Brain Research, in press

Questions regarding the appropriateness of facial expressions in particular situations arise ubiquitously in everyday social interactions. To determine the appropriateness of facial affect, first of all, we should represent our own or the other's emotional state as induced by the social situation. Then, based on these representations, we should infer the possible affective response of the other person. In this study, we identified the brain mechanism mediating special types of social evaluative judgments of facial affect in which the internal reference is related to theory of mind (ToM) processing. Many previous ToM studies have used non-emotional stimuli, but, because so much valuable social information is conveyed through nonverbal emotional channels, this investigation used emotionally salient visual materials to tap ToM. Fourteen right-handed healthy subjects volunteered for our study. We used functional magnetic resonance imaging to examine brain activation during the judgmental task for the appropriateness of facial affects as opposed to gender matching tasks. We identified activation of a brain network, which includes both medial frontal cortex, left temporal pole, left inferior frontal gyrus, and left thalamus during the judgmental task for appropriateness of facial affect compared to the gender matching task. The results of this study suggest that the brain system involved in ToM plays a key role in judging the appropriateness of facial affect in an emotionally laden situation. In addition, our result supports that common neural substrates are involved in performing diverse kinds of ToM tasks irrespective of perceptual modalities and the emotional salience of test materials.

ARTICLE UPDATE - How positive affect modulates cognitive control: The costs and benefits of reduced maintenance capability.

Dreisbach G

Brain and Cognition, in press

Adaptive action in a constantly changing environment requires the ability to maintain intentions and goals over time and to flexibly switch between these goals in response to significant changes. argued that positive affect modulates these antagonistic control demands in favor of a more flexible but also more distractible behavior. In the present paper, the author will present further evidence for the affective modulation of cognitive control: mild positive affect reduced maintenance capability in a simple cuing paradigm (the AX Continuous Performance Task) as compared to negative and neutral affect. This reduced maintenance capability results in costs when a to be maintained goal has to be executed and conversely results in benefits when a to be maintained goal unexpectedly changes. The data will be discussed with respect to existing theories on positive affect, cognitive control, and dopamine.

ARTICLE UPDATE - Bridging emotion theory and neurobiology through dynamic systems modeling

Lewis MD.

Behavioral and Brain Sciences, 28, 169-245.

Efforts to bridge emotion theory with neurobiology can be facilitated by dynamic systems (DS) modeling. DS principles stipulate higher-order wholes emerging from lower-order constituents through bidirectional causal processes--offering a common language for psychological and neurobiological models. After identifying some limitations of mainstream emotion theory, I apply DS principles to emotion-cognition relations. I then present a psychological model based on this reconceptualization, identifying trigger, self-amplification, and self-stabilization phases of emotion-appraisal states, leading to consolidating traits. The article goes on to describe neural structures and functions involved in appraisal and emotion, as well as DS mechanisms of integration by which they interact. These mechanisms include nested feedback interactions, global effects of neuromodulation, vertical integration, action-monitoring, and synaptic plasticity, and they are modeled in terms of both functional integration and temporal synchronization. I end by elaborating the psychological model of emotion-appraisal states with reference to neural processes.

ARTICLE UPDATE - Modulation of retrieval processing reflects accuracy of emotional source memory.

Smith AP, Henson RN, Rugg MD, Dolan RJ.

Learning & Memory, 12, 427-429.

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.

ARTICLE UPDATE - Analysis of Single-Unit Responses to Emotional Scenes in Human Ventromedial Prefrontal Cortex

Hiroto Kawasaki, Ralph Adolphs, Hiroyuki Oya, Christopher Kovach, Hanna Damasio, Olaf Kaufman and Matthew Howard, III

Journal of Cognitive Neuroscience, 17, 1509-1518.

Lesion and functional imaging studies in humans have shown that the ventral and medial prefrontal cortex is critically involved in the processing of emotional stimuli, but both of these methods have limited spatiotemporal resolution. Conversely, neurophysiological studies of emotion in nonhuman primates typically rely on stimuli that do not require elaborate cognitive processing. To begin bridging this gap, we recorded from a total of 267 neurons in the left and right orbital and anterior cingulate cortices of four patients who had chronically implanted depth electrodes for monitoring epilepsy. Peristimulus activity was recorded to standardized, complex visual scenes depicting neutral, pleasant, or aversive content. Recording locations were verified with postoperative magnetic resonance imaging. Using a conservative, multistep statistical evaluation, we found significant responses in 56 neurons; 16 of these were selective for only one emotion class, most often aversive. The findings suggest sparse and widely distributed processing of emotional value in the prefrontal cortex, with a predominance of responses to aversive stimuli.

ARTICLE UPDATE - Attentional Bias to Pictures of Fear-Relevant Animals in a Dot Probe Task

Lipp, O. V., & Derakshan, N.

Emotion, 5, 365-369.

Attentional bias to fear-relevant animals was assessed in 69 participants not preselected on self-reported anxiety with the use of a dot probe task showing pictures of snakes, spiders, mushrooms, and flowers. Probes that replaced the fear-relevant stimuli (snakes and spiders) were found faster than probes that replaced the non-fear-relevant stimuli, indicating an attentional bias in the entire sample. The bias was not correlated with self-reported state or trait anxiety or with general fearfulness. Participants reporting higher levels of spider fear showed an enhanced bias to spiders, but the bias remained significant in low scorers. The bias to snake pictures was not related to snake fear and was significant in high and low scorers. These results indicate preferential processing of fear-relevant stimuli in an unselected sample.

ARTICLE UPDATE - The Role of Fear-Relevant Stimuli in Visual Search: A Comparison of Phylogenetic and Ontogenetic Stimuli

Brosch, T., & Sharma, D.

Emotion, 5, 360-364.

It has been argued that phylogenetic fear-relevant stimuli elicit preattentive capture of attention. To distinguish between fear relevance and time of appearance in evolutionary history, the authors compare phylogenetic and ontogenetic fear-relevant and fear-irrelevant stimuli in a visual search task. The authors found no evidence for a special role of phylogenetic fear-relevant stimuli; it seems that fear relevance in general is more important than is the evolutionary age. The pattern of results indicates that attention toward threatening stimuli is mainly affected by a late component that prolongs the disengagement of attention.

ARTICLE UPDATE - Visual Search With Biological Threat Stimuli: Accuracy, Reaction Times, and Heart Rate Changes

Anders Flykt

Emotion, 5, 349-353.

Twenty-four participants were given a visual search task of deciding whether all the pictures in 3 × 3 search arrays contained a target picture from a deviant category, and heart rate was measured. The categories were snakes, spiders, flowers, and mushrooms. Shorter reaction times (RTs) were observed for fear-relevant (snake and spider) targets rather than for fear-irrelevant/neutral (flower and mushroom) targets. This difference was most pronounced for the participants presented with a gray-scale version of the search arrays. The 1st interbeat interval (IBI), after the search array onset, showed an effect of the target, whereas the 2nd IBI also showed an effect of the distractors. The results suggest that controlled processing of the task operates together with automatic processing.

ARTICLE UPDATE - Integrated neural representations of odor intensity and affective valence in human amygdala.

Winston JS, Gottfried JA, Kilner JM, Dolan RJ.

Journal of Neuroscience, 25, 8903-8907.

Arousal and valence are proposed to represent fundamental dimensions of emotion. The neural substrates for processing these aspects of stimuli are studied widely, with recent studies of chemosensory processing suggesting the amygdala processes intensity (a surrogate for arousal) rather than valence. However, these investigations have assumed that a valence effect in the amygdala is linear such that testing valence extremes is sufficient to infer responses across valence space. In this study, we tested an alternative hypothesis, namely that valence responses in the amygdala are nonlinear. Using event-related functional magnetic resonance imaging, we measured amygdala responses to high- and low-concentration variants of pleasant, neutral, and unpleasant odors. Our results demonstrate that the amygdala exhibits an intensity-by-valence interaction in olfactory processing. In other words, the effect of intensity on amygdala activity is not the same at all levels of valence. Specifically, the amygdala responds differentially to high (vs low)-intensity odor for pleasant and unpleasant smells but not for neutral smells. This implies that the amygdala codes neither intensity nor valence per se, but a combination that we suggest reflects the overall emotional value of a stimulus.