ARTICLE UPDATE - Attentional load affects automatic emotional processing: evidence from event-related potentials.

Doallo S, Holguin SR, Cadaveira F.

Neuroreport, 17, 1797-1801

One open question on the relation between attention and emotion concerns the automatic processing of emotional visual stimuli outside the focus of attention. This study examined to what extent the emotional processing at unattended locations is modulated by the processing load at attended locations. Event-related potentials were measured to task-irrelevant unpleasant and neutral pictures briefly presented at peripheral locations while participants performed a visual central task varying in load (low and high load). Unpleasant pictures elicited larger amplitudes of N1-P2 at parietoccipital and occipital sites than that of neutral pictures. This effect was only significant in the low-load condition. Data suggest that brain responses to affective value of task-irrelevant peripheral pictures are modulated by attentional load at fixation.

ARTICLE UPDATE - Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala

H.T. Ghashghaei, 1, C.C. Hilgetag, d and H. Barbas

NeuroImage, in press

The prefrontal cortex and the amygdala have synergistic roles in regulating purposive behavior, effected through bidirectional pathways. Here we investigated the largely unknown extent and laminar relationship of prefrontal input–output zones linked with the amygdala using neural tracers injected in the amygdala in rhesus monkeys. Prefrontal areas varied vastly in their connections with the amygdala, with the densest connections found in posterior orbitofrontal and posterior medial cortices, and the sparsest in anterior lateral prefrontal areas, especially area 10. Prefrontal projection neurons directed to the amygdala originated in layer 5, but significant numbers were also found in layers 2 and 3 in posterior medial and orbitofrontal cortices. Amygdalar axonal terminations in prefrontal cortex were most frequently distributed in bilaminar bands in the superficial and deep layers, by columns spanning the entire cortical depth, and less frequently as small patches centered in the superficial or deep layers. Heavy terminations in layers 1–2 overlapped with calbindin-positive inhibitory neurons. A comparison of the relationship of input to output projections revealed that among the most heavily connected cortices, cingulate areas 25 and 24 issued comparatively more projections to the amygdala than they received, whereas caudal orbitofrontal areas were more receivers than senders. Further, there was a significant relationship between the proportion of ‘feedforward’ cortical projections from layers 2–3 to ‘feedback’ terminations innervating the superficial layers of prefrontal cortices. These findings indicate that the connections between prefrontal cortices and the amygdala follow similar patterns as corticocortical connections, and by analogy suggest pathways underlying the sequence of information processing for emotions.

ARTICLE UPDATE - The impact of processing load on emotion.

D.G.V. Mitchell, M. Nakic, D. Fridberg, N. Kamel, D.S. Pine and R.J.R. Blair

NeuroImage, in press

This event-related fMRI study examined the impact of processing load on the BOLD response to emotional expressions. Participants were presented with composite stimuli consisting of neutral and fearful faces upon which semi-transparent words were superimposed. This manipulation held stimulus-driven features constant across multiple levels of processing load. Participants made either (1) gender discriminations based on the face; (2) case judgments based on the words; or (3) syllable number judgments based on the words. A significant main effect for processing load was revealed in prefrontal cortex, parietal cortex, visual processing areas, and amygdala. Critically, enhanced activity in the amygdala and medial prefrontal cortex seen during gender discriminations was significantly reduced during the linguistic task conditions. A connectivity analysis conducted to investigate theories of cognitive modulation of emotion showed that activity in dorsolateral prefrontal cortex was inversely related to activity in the ventromedial prefrontal cortex. Together, the data suggest that the processing of task-irrelevant emotional information, like neutral information, is subject to the effects of processing load and is under top-down control.

ARTICLE UPDATE - Emotional memories are not all created equal: Evidence for selective memory enhancement

Adam K. Anderson, Yuki Yamaguchi, Wojtek Grabski, and Dominika Lacka

LEARNING & MEMORY, 13, 711-718

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

ARTICLE UPDATE - Regulation of emotional responses elicited by threat-related stimuli.

Eippert F, Veit R, Weiskopf N, Erb M, Birbaumer N, Anders S.

Human Brain Mapping, in press

The capacity to voluntarily regulate emotions is critical for mental health, especially when coping with aversive events. Several neuroimaging studies of emotion regulation found the amygdala to be a target for downregulation and prefrontal regions to be associated with downregulation. To characterize the role of prefrontal regions in bidirectional emotion regulation and to investigate regulatory influences on amygdala activity and peripheral physiological measures, a functional magnetic resonance imaging (fMRI) study with simultaneous recording of self-report, startle eyeblink, and skin conductance responses was carried out. Subjects viewed threat-related pictures and were asked to up- and downregulate their emotional responses using reappraisal strategies. While startle eyeblink responses (in successful regulators) and skin conductance responses were amplified during upregulation, but showed no consistent effect during downregulation, amygdala activity was increased and decreased according to the regulation instructions. Trial-by-trial ratings of regulation success correlated positively with activity in amygdala during upregulation and orbitofrontal cortex during downregulation. Downregulation was characterized by left-hemispheric activation peaks in anterior cingulate cortex, dorsolateral prefrontal cortex, and orbitofrontal cortex and upregulation was characterized by a pattern of prefrontal activation not restricted to the left hemisphere. Further analyses showed significant overlap of prefrontal activation across both regulation conditions, possibly reflecting cognitive processes underlying both up- and downregulation, but also showed distinct activations in each condition. The present study demonstrates that amygdala responses to threat-related stimuli can be controlled through the use of cognitive strategies depending on recruitment of prefrontal areas, thereby changing the subject's affective state.

ARTICLE UPDATE - An electrophysiological study on the interaction between emotional content and spatial frequency of visual stimuli

Luis Carretié, José A. Hinojosa, Sara López-Martín and Manuel Tapia

Neuropsychologia, in press

Previous studies suggest that the magnocellular pathway, a visual processing system that rapidly provides low spatial frequency information to fast-responding structures such as the amygdala, is more involved in the processing of emotional facial expressions than the parvocellular pathway (which conveys all spatial frequencies). The present experiment explored the spatio-temporal characteristics of the spatial frequency modulation of affect-related neural processing, as well as its generalizability to non-facial stimuli. To that aim, the event-related potentials (ERPs) elicited by low-pass filtered (i.e., high spatial frequencies are eliminated) and intact non-facial emotional images were recorded from 31 participants using a 60-electrode array. The earliest significant effect of spatial frequency was observed at 135 ms from stimulus onset: N135 component of the ERPs. In line with previous studies, the origin of N135 was localized at secondary visual areas for low-pass filtered stimuli and at primary areas for intact stimuli. Importantly, this component showed an interaction between spatial frequency and emotional content: within low-pass filtered pictures, negative stimuli elicited the highest N135 amplitudes. By contrast, within intact stimuli, neutral pictures were those eliciting the highest amplitudes. These results suggest that high spatial frequencies are not essential for the initial affect-related processing of visual stimuli, which would mainly rely on low spatial frequency visual information. According to present data, high spatial frequencies would come into play later on.

ARTICLE UPDATE - Is this happiness I see? Biases in the identification of emotional facial expressions in depression and social phobia.

Joormann J, Gotlib IH.

Journal of Abnormal Psychology, 115, 705-714.

The present study was designed to examine the operation of depression-specific biases in the identification or labeling of facial expression of emotions. Participants diagnosed with major depression and social phobia and control participants were presented with faces that expressed increasing degrees of emotional intensity, slowly changing from a neutral to a full-intensity happy, sad, or angry expression. The authors assessed individual differences in the intensity of facial expression of emotion that was required for the participants to accurately identify the emotion being expressed. The depressed participants required significantly greater intensity of emotion than did the social phobic and the control participants to correctly identify happy expressions and less intensity to identify sad than angry expressions. In contrast, social phobic participants needed less intensity to correctly identify the angry expressions than did the depressed and control participants and less intensity to identify angry than sad expressions. Implications of these results for interpersonal functioning in depression and social phobia are discussed.

ARTICLE UPDATE - Green love is ugly: Emotions elicited by synesthetic grapheme-color perceptions.

Callejas A, Acosta A, Lupianez J.

Brain Research, in press

Synesthetes who experience grapheme-color synesthesia often report feeling uneasy when dealing with incongruently colored graphemes although no empirical data is available to confirm this phenomenon. We studied this affective reaction related to synesthetic perceptions by means of an evaluation task. We found that the perception of an incorrectly colored word affects the judgments of emotional valence. Furthermore, this effect competed with the word's emotional valence in a categorization task thus supporting the automatic nature of this synesthetically elicited affective reaction. When manipulating word valence and word color-photism congruence, we found that responses were slower (and less accurate) for inconsistent conditions than for consistent conditions. Inconsistent conditions were defined as those where semantics and color-photism congruence did not produce a similar assessment and therefore gave rise to a negative affective reaction (i.e., positive-valence words presented in a color different from the synesthete's photism or negative-valence words presented in the photism's color). We therefore observed a modulation of the congruency effect (i.e., faster reaction times to congruently colored words than incongruently colored words). Although this congruence effect has been taken as an index of the true experience of synesthesia, we observed that it can be reversed when the experimental manipulations turn an incongruently colored word into a consistent stimulus. To our knowledge, this is the first report of an affective reaction elicited by the congruency between the synesthetically induced color of a word and the color in which the word is actually presented. The underlying neural mechanisms that might be involved in this phenomenon are discussed.

ARTICLE UPDATE - Recent fear is resistant to extinction

Stephen Maren and Chun-hui Chang

PNAS, 103, 18020-18025

In some individuals, fearful experiences (e.g., combat) yield persistent and debilitating psychological disturbances, including posttraumatic stress disorder (PTSD). Early intervention (e.g., debriefing) after psychological trauma is widely practiced and argued to be an effective strategy for limiting subsequent psychopathology, although there has been considerable debate on this point. Here we show in an animal model of traumatic fear that early intervention shortly after an aversive experience yields poor long-term fear reduction. Extinction trials administered minutes after aversive fear conditioning in rats suppressed fear acutely, but fear suppression was not maintained the next day. In contrast, delivering extinction trials 1 day after fear conditioning produced an enduring suppression of fear memory. We further show that the recent experience of an aversive event, not the timing of the extinction intervention per se, inhibits the development of long-term fear extinction. These results reveal that the level of fear present at the time of intervention is a critical factor in the efficacy of extinction. Importantly, our work suggests that early intervention may not yield optimal outcomes in reducing posttraumatic stress, particularly after severe trauma.

ARTICLE UPDATE - Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG

Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG

Qian Luo, Tom Holroyd, Matthew Jones, Talma Hendler, and James Blair

NeuroImage, in press

Facial threat conveys important information about imminent environmental danger. The rapid detection of this information is critical for survival and social interaction. However, due to technical and methodological difficulties, the spatiotemporal profile for facial threat processing is unknown. By utilizing magnetoencephalography (MEG), a brain-imaging technique with superb temporal resolution and fairly good spatial resolution, Synthetic Aperture Magnetometry (SAM), a recently developed source analysis technique, and a sliding window analysis, we identified the spatiotemporal development of facial threat processing in the gamma frequency band. We also tested the dual-route hypothesis by LeDoux who proposed, based on animal research, that there are two routes to the amygdala: a quick subcortical route and a slower and cortical route. Direct evidence with humans supporting this model has been lacking. Moreover, it has been unclear whether the subcortical route responds specifically to fearful expressions or to threatening expressions in general. We found early event-related synchronizations (ERS) in response to fearful faces in the hypothalamus/thalamus area (10–20 ms) and then the amygdala (20–30 ms). This was even earlier than the ERS response seen to fearful faces in visual cortex (40–50 ms). These data support LeDoux's suggestion of a quick, subcortical thamalo-amygdala route. Moreover, this route was specific for fear expressions; the ERS response in the amygdala to angry expressions had a late onset (150–160 ms). The ERS onset in prefrontal cortex followed that seen within the amygdala (around 160–210 ms). This is consistent with its role in higher-level emotional/cognitive processing.

ARTICLE UPDATE - Mood Alters Amygdala Activation to Sad Distractors During an Attentional Task

Lihong Wang, Kevin S. LaBar and Gregory McCarthy

Biological Psychiatry, 60, 1139-1146

Background

A behavioral hallmark of mood disorders is biased perception and memory for sad events. The amygdala is poised to mediate internal mood and external event processing because of its connections with both the internal milieu and the sensory world. There is little evidence showing that the amygdala’s response to sad sensory stimuli is functionally modulated by mood state, however.
Methods

We investigated the impact of mood on amygdala activation evoked by sad and neutral pictures presented as distractors during an attentional oddball task. Healthy adults underwent functional magnetic resonance imaging during task runs that were preceded by sad or happy movie clips. Happy and sad mood induction was conducted within-subjects on consecutive days in counterbalanced order.
Results

Amygdala activation to sad distractors was enhanced after viewing sad movies relative to happy ones and was correlated with reaction time costs to detect attentional targets. The activation was higher in female subjects in the right hemisphere. The anterior cingulate, ventromedial and orbital prefrontal cortex, insula, and other posterior regions also showed enhanced responses to sad distractors during sad mood.
Conclusions

These findings reveal brain mechanisms that integrate emotional input and current mood state, with implications for understanding cognitive distractibility in depression.

ARTICLE UPDATE - Detecting fearful and neutral faces: BOLD latency differences in amygdala–hippocampal junction

A.A.T.S. Reinders, J. Gläscher, J.R. de Jong, A.T.M. Willemsen, J.A. den Boer and C. Büchel

NeuroImage, 33, 805-814

Evolutionary survival and procreation are augmented if an individual organism quickly detects environmental threats and rapidly initiates defensive behavioral reactions. Thus, facial emotions signaling a potential threat, e.g., fear or anger, should be perceived rapidly and automatically, possibly through a subcortical processing route which includes the amygdala. Using event-related functional magnetic resonance imaging (fMRI), we investigated the time course of the response in the amygdala to neutral and fearful faces, which appear from dynamically decreasing random visual noise. We aimed to detect differences of the amygdala response between fearful and neutral faces by estimating the latency of the blood oxygenation level-dependent (BOLD) response. We found that bilateral amygdala–hippocampal junction activation occurred earlier for fearful than for neutral faces. Our findings support the theory of a dual route architecture in which the subcortical thalamic–hippocampal–amygdala route serves fast preconscious threat perception.

ARTICLE UPDATE - A gender- and sexual orientation-dependent spatial attentional effect of invisible images

Yi Jiang, Patricia Costello, Fang Fang, Miner Huang, and Sheng He

PNAS, 103, 17048-17052

Human observers are constantly bombarded with a vast amount of information. Selective attention helps us to quickly process what is important while ignoring the irrelevant. In this study, we demonstrate that information that has not entered observers' consciousness, such as interocularly suppressed (invisible) erotic pictures, can direct the distribution of spatial attention. Furthermore, invisible erotic information can either attract or repel observers' spatial attention depending on their gender and sexual orientation. While unaware of the suppressed pictures, heterosexual males' attention was attracted to invisible female nudes, heterosexual females' attention was attracted to invisible male nudes, gay males behaved similarly to heterosexual females, and gay/bisexual females performed in-between heterosexual males and females.

ARTICLE UPDATE - Emotional modulation of pain: is it the sensation or what we recall?

Godinho F, Magnin M, Frot M, Perchet C, Garcia-Larrea L.

Journal of Neuroscience, 26, 11454-11461

Emotions modulate pain perception, although the mechanisms underlying this phenomenon remain unclear. In this study, we show that intensity reports significantly increased when painful stimuli were concomitant to images showing human pain, whereas pictures with identical emotional values but without somatic content failed to modulate pain. Early somatosensory responses (<200 ms) remained unmodified by emotions. Conversely, late responses showed a significant enhancement associated with increased pain ratings, localized to the right prefrontal, right temporo-occipital junction, and right temporal pole. In contrast to selective attention, which enhances pain ratings by increasing sensory gain, emotions triggered by seeing other people's pain did not alter processing in SI-SII (primary and second somatosensory areas), but may have biased the transfer to, and the representation of pain in short-term memory buffers (prefrontal), as well as the affective assignment to this representation (temporal pole). Memory encoding and recall, rather than sensory processing, appear to be modulated by empathy with others' physical suffering.

ARTICLE UPDATE - Time course of amygdala activation during aversive conditioning

Thomas Straube, Thomas Weiss, Hans-Joachim Mentzel, and Wolfgang H.R. Miltner

NeuroImage, in press

The time course of amygdala activation during aversive conditioning is a matter of debate. While some researchers reported rapid habituation, others found stable or no amygdalar responses to conditioned stimuli at all. In the present event-related fMRI study, we investigated whether the activity of the amygdala during aversive conditioning depends on attentional conditions. Subjects underwent aversive delay conditioning by pairing an electrical shock (unconditioned aversive stimulus) with a visual conditioned stimulus (CS+). For each singular presentation of the CS+ or a nonconditioned visual stimulus (CS−), subjects attended in random order to features that either differed between both stimuli (identification task) or that did not differ (distraction task). For the identification task trials, increased responses of the left amygdala to CS+ versus CS− were rapidly established but absent at the end of the conditioning trials. In contrast, under the distraction condition,
amygdala activation to CS+ versus CS− was present during the late but not the early phase of conditioning. The results suggest that the time course of amygdala activity during aversive associative learning is strongly modulated by an interaction of attention and time.

ARTICLE UPDATE - Time-locked brain activity associated with emotion: a pilot MEG study.

Leon-Carrion J, McManis MH, Castillo EM, Papanicolaou AC.

Brain Injury, in press

To examine the time course of brain activation in response to emotionally evocative pictures. METHODS AND PROCEDURES: Regions of the brain involved in the processing of affective stimuli in response to picture sets rated unpleasant, pleasant and affectively neutral, as well as the order of activation of each region, were investigated using magnetoencephalography in 10 normal adult volunteers. RESULTS: Spatiotemporal maps were found consisting of two basic components. The first involving activation in the occipital and basal aspects of the temporal cortex- lasted, on average, 270 ms post-stimulus. The second component involving activation in the mesial temporal lobes (MTL) extended from 270 to 850 ms post-stimulus. After (serial) activating the mesial temporal lobe structures or simultaneous (parallel) to it, activation is also observed in the frontal structures. CONCLUSIONS: The temporal organization in the brain of an emotional stimulus requires the serial and alternating engagement of frontal and posterior cortices. It is suggested that lesions to the brain may disrupt this temporal course, altering the emotional response commonly observed in patients with brain injury.

ARTICLE UPDATE - Sex differences in brain activation patterns during processing of positively and negatively valenced emotional words

Hofer A, Siedentopf CM, Ischebeck A, Rettenbacher MA, Verius M, Felber S, Wolfgang Fleischhacker W.

Psychological Medicine, in press

Background. Previous studies have suggested that men and women process emotional stimuli differently. In this study, we used event-related functional magnetic resonance imaging (fMRI) to investigate gender differences in regional cerebral activity during the perception of positive or negative emotions.

Method. The experiment comprised two emotional conditions (positively/negatively valenced words) during which fMRI data were acquired.

Results. Thirty-eight healthy volunteers (19 males, 19 females) were investigated. A direct comparison of brain activation between men and women revealed differential activation in the right putamen, the right superior temporal gyrus, and the left supramarginal gyrus during processing of positively valenced words versus non-words for women versus men. By contrast, during processing of negatively valenced words versus non-words, relatively greater activation was seen in the left perirhinal cortex and hippocampus for women versus men, and in the right supramarginal gyrus for men versus women.

Conclusions. Our findings suggest gender-related neural responses to emotional stimuli and could contribute to the understanding of mechanisms underlying the gender disparity of neuropsychiatric diseases such as mood disorders.

ARTICLE UPDATE - Preferential responses in amygdala and insula during presentation of facial contempt and disgust.

Fabio Sambataro, Savino Dimalta, Annabella Di Giorgio, Paolo Taurisano, Giuseppe Blasi, Tommaso Scarabino, Giuseppe Giannatempo, Marcello Nardini and Alessandro Bertolino

European Journal of Neuroscience, in press

Some authors consider contempt to be a basic emotion while others consider it a variant of disgust. The neural correlates of contempt have not so far been specifically contrasted with disgust. Using functional magnetic resonance imaging (fMRI), we investigated the neural networks involved in the processing of facial contempt and disgust in 24 healthy subjects. Facial recognition of contempt was lower than that of disgust and of neutral faces. The imaging data indicated significant activity in the amygdala and in globus pallidus and putamen during processing of contemptuous faces. Bilateral insula and caudate nuclei and left as well as right inferior frontal gyrus were engaged during processing of disgusted faces. Moreover, direct comparisons of contempt vs. disgust yielded significantly different activations in the amygdala. On the other hand, disgusted faces elicited greater activation than contemptuous faces in the right insula and caudate. Our findings suggest preferential involvement of different neural substrates in the processing of facial emotional expressions of contempt and disgust.

ARTICLE UPDATE - Individual differences in amygdala activity predict response speed during working memory.

Schaefer A, Braver TS, Reynolds JR, Burgess GC, Yarkoni T, Gray JR.

The Journal of Neuroscience, 26, 12120-12128

The human amygdala has classically been viewed as a brain structure primarily related to emotions and dissociated from higher cognition. We report here findings suggesting that the human amygdala also has a role in supporting working memory (WM), a canonical higher cognitive function. In a first functional magnetic resonance imaging (fMRI) study (n = 53), individual differences in amygdala activity predicted behavioral performance in a 3-back WM task. Specifically, higher event-related amygdala amplitude predicted faster response time (RT; r = -0.64), with no loss of accuracy. This relationship was not contingent on mood state, task content, or personality variables. In a second fMRI study (n = 21), we replicated the key finding (r = -0.47) and further showed that the correlation between the amygdala and faster RT was specific to a high working memory load condition (3-back) compared with a low working memory load condition (1-back). These results support models of amygdala function that can account for its involvement not only in emotion but also higher cognition.

ARTICLE UPDATE - Effects of emotional arousal on multiple memory systems: Evidence from declarative and procedural learning

Stephan Steidl, Salwa Mohi-uddin and Adam K. Anderson

Learning and Memory, in press

Extensive evidence documents emotional modulation of hippocampus-dependent declarative memory in humans. However, little is known about the emotional modulation of striatum-dependent procedural memory. To address how emotional arousal influences declarative and procedural memory, the current study utilized (1) a picture recognition and (2) a weather prediction (WP) task (a probabilistic classification learning task), which have been shown to rely on hippocampal- and striatum-based memory systems, respectively. Observers viewed arousing or neutral pictures after (Experiment 1) or during (Experiment 2) WP training trials. A 1-wk delayed picture recognition memory test revealed enhanced declarative memory for arousing compared with neutral pictures. Arousal during encoding impaired initial WP acquisition but did not influence retention when tested after a 1-wk delay. Data from a subsequent 3-mo delayed test, however, suggested that arousal during acquisition may enhance remote WP retention. These results suggest a potential dissociation between how readily emotional arousal influences hippocampus-dependent and striatum-dependent memory systems in humans.