Neural responses to happy,fearful and angry faces of varying identities in 5- and 7-month-old infants

The processing of facial emotion is an important social skill that develops throughout infancy and early childhood. Here we investigate the neural underpinnings of the ability to process facial emotion across changes in facial identity in cross-sectional groups of 5- and 7-month-old infants. We simultaneously measured neural metabolic, behavioral, and autonomic responses to happy, fearful, and angry faces of different female models using functional near-infrared spectroscopy (fNIRS), eye-tracking, and heart rate measures. We observed significant neural activation to these facial emotions in a distributed set of frontal and temporal brain regions, and longer looking to the mouth region of angry faces compared to happy and fearful faces. No differences in looking behavior or neural activations were observed between 5- and 7-month-olds, although several exploratory, age-independent associations between neural activations and looking behavior were noted. Overall, these findings suggest more developmental stability than previously thought in responses to emotional facial expressions of varying identities between 5- and 7-months of age.     

Trait and state corticostriatal dysfunction in bipolar disorder during emotional face processing

Liu J, Blond BN, van Dyck LI, Spencer L, Wang F, Blumberg HP. Trait and state corticostriatal dysfunction in bipolar disorder during emotional face processing.
Bipolar Disord 2012: 14: 432–441. © 2012 The Authors. Journal compilation © 2012 John Wiley & Sons A/S. Objectives: Convergent evidence supports limbic, anterior paralimbic, and prefrontal cortex (PFC) abnormalities in emotional processing in bipolar disorder (BD) and suggests that some abnormalities are mood‐state dependent and others persist into euthymia. However, few studies have assessed elevated, depressed, and euthymic mood states while individuals processed emotional stimuli of varying valence to investigate trait‐ and state‐related neural system responses. Here, regional brain responses to positive, negative, and neutral emotional stimuli were assessed in individuals with BD during elevated, depressed, and euthymic mood states. Methods: One hundred and thirty‐four subjects participated in functional magnetic resonance imaging scanning while processing faces depicting happy, fearful, and neutral expressions: 76 with BD (18 in elevated mood states, 19 depressed, 39 euthymic) and 58 healthy comparison (HC) individuals. Analyses were performed for BD trait‐ and mood state‐related features. Results: Ventral anterior cingulate cortex (VACC), orbitofrontal cortex (OFC), and ventral striatum responses to happy and neutral faces were decreased in the BD group, compared to the HC group, and were not influenced by mood state. Elevated mood states were associated with decreased right rostral PFC activation to fearful and neutral faces, and depression was associated with increased left OFC activation to fearful faces. Conclusions: The findings suggest that abnormal VACC, OFC, and ventral striatum responses to happy and neutral stimuli are trait features of BD. Acute mood states may be associated with additional lateralized abnormalities of diminished right rostral PFC responses to fearful and neutral stimuli in elevated states and increased left OFC responses to fearful stimuli in depressed states.     

Age‐related changes in amygdala–frontal connectivity during emotional face processing from childhood into young adulthood

The ability to process and respond to emotional facial expressions is a critical skill for healthy social and emotional development. There has been growing interest in understanding the neural circuitry underlying development of emotional processing, with previous research implicating functional connectivity between amygdala and frontal regions. However, existing work has focused on threatening emotional faces, raising questions regarding the extent to which these developmental patterns are specific to threat or to emotional face processing more broadly. In the current study, we examined age‐related changes in brain activity and amygdala functional connectivity during an fMRI emotional face matching task (including angry, fearful, and happy faces) in 61 healthy subjects aged 7–25 years. We found age‐related decreases in ventral medial prefrontal cortex activity in response to happy faces but not to angry or fearful faces, and an age‐related change (shifting from positive to negative correlation) in amygdala–anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC) functional connectivity to all emotional faces. Specifically, positive correlations between amygdala and ACC/mPFC in children changed to negative correlations in adults, which may suggest early emergence of bottom‐up amygdala excitatory signaling to ACC/mPFC in children and later development of top‐down inhibitory control of ACC/mPFC over amygdala in adults. Age‐related changes in amygdala–ACC/mPFC connectivity did not vary for processing of different facial emotions, suggesting changes in amygdala–ACC/mPFC connectivity may underlie development of broad emotional processing, rather than threat‐specific processing. Hum Brain Mapp 37:1684–1695, 2016. © 2016 Wiley Periodicals, Inc .     

Emotional facial expressions modulate pain-induced beta and gamma oscillations in sensorimotor cortex

Painful events in our environment are often accompanied by stimuli from other sensory modalities. These stimuli may influence the perception and processing of acute pain, in particular when they comprise emotional cues, like facial expressions of people surrounding us. In this whole-head magnetoencephalography (MEG) study, we examined the neuronal mechanisms underlying the influence of emotional (fearful, angry, or happy) compared to neutral facial expressions on the processing of pain in humans. Independent of their valence, subjective pain ratings for intracutaneous inputs were higher when pain stimuli were presented together with emotional facial expressions than when they were presented with a neutral facial expression. Source reconstruction using linear beamforming revealed pain-induced early (70-270 ms) oscillatory beta-band activity (BBA; 15-25 Hz) and gamma-band activity (GBA; 60-80 Hz) in the sensorimotor cortex. The presentation of faces with emotional expressions compared to faces with neutral expressions led to a stronger bilateral suppression of the pain-induced BBA, possibly reflecting enhanced response readiness of the sensorimotor system. Moreover, pain-induced GBA in the sensorimotor cortex was larger for faces expressing fear than for faces expressing anger, which might reflect the facilitation of avoidance-motivated behavior triggered by the concurrent presentation of faces with fearful expressions and painful stimuli. Thus, the presence of emotional cues, like facial expressions from people surrounding us, while receiving acute pain may facilitate neuronal processes involved in the preparation and execution of adequate protective motor responses.     

A developmental examination of gender differences in brain engagement during evaluation of threat.

BACKGROUND: Females appear to be more sensitive and responsive to social cues, including threat signals, than are males. Recent theoretical models suggest that developmental changes in brain functioning play important roles in the emergence of such gender differences. METHODS: We used functional magnetic resonance imaging to examine developmental and gender differences in activation of neural structures thought to mediate attention to emotional faces depicting varying degrees of threat. Analyses focused on the orbitofrontal cortex, amygdala, and anterior cingulate cortex during the evaluation of threat conveyed by faces. Healthy adolescents (n = 17; 53% male) and adults (n = 17; 53% male) were scanned while they rated how threatening pictures of neutral and emotional (angry, fearful, or happy) faces appeared. RESULTS: Results indicate significant interactions among age, gender, and face type for activation during explicit threat monitoring. In particular, adult women activated orbitofrontal cortex and amygdala selectively to unambiguous threat (angry) cues, while adult men showed a less discriminating pattern of activation. No gender differences were evident for adolescents, who as a group resembled adult males. CONCLUSIONS: These findings suggest that there are gender differences in patterns of neural responses to emotional faces that are not fully apparent until adulthood.     

Recognition advantage of happy faces: Tracing the neurocognitive processes

The present study aimed to identify the brain processes—and their time course—underlying the typical behavioral recognition advantage of happy facial expressions. To this end, we recorded EEG activity during an expression categorization task for happy, angry, fearful, sad, and neutral faces, and the correlation between event-related-potential (ERP) patterns and recognition performance was assessed. N170 (150–180 ms) was enhanced for angry, fearful and sad faces; N2 was reduced and early posterior negativity (EPN; both, 200–320 ms) was enhanced for happy and angry faces; P3b (350–450 ms) was reduced for happy and neutral faces; and slow positive wave (SPW; 700–800 ms) was reduced for happy faces. This reveals (a) an early processing (N170) of negative affective valence (i.e., angry, fearful, and sad), (b) discrimination (N2 and EPN) of affective intensity or arousal (i.e., angry and happy), and (c) facilitated categorization (P3b) and decision (SPW) due to expressive distinctiveness (i.e., happy). In addition, N2, EPN, P3b, and SPW were related to categorization accuracy and speed. This suggests that conscious expression recognition and the typical happy face advantage depend on encoding of expressive intensity and, especially, on later response selection, rather than on the early processing of affective valence.     

Frontolimbic responses to emotional face memory: The neural correlates of first impressions

First impressions, especially of emotional faces, may critically impact later evaluation of social interactions. Activity in limbic regions, including the amygdala and ventral striatum, has previously been shown to correlate with identification of emotional content in faces; however, little work has been done describing how these signals may influence emotional face memory. We report an event‐related functional magnetic resonance imaging study in 21 healthy adults where subjects attempted to recognize a neutral face that was previously viewed with a threatening (angry or fearful) or nonthreatening (happy or sad) affect. In a hypothesis‐driven region of interest analysis, we found that neutral faces previously presented with a threatening affect recruited the left amygdala. In contrast, faces previously presented with a nonthreatening affect activated the left ventral striatum. A whole‐brain analysis revealed increased response in the right orbitofrontal cortex to faces previously seen with threatening affect. These effects of prior emotion were independent of task performance, with differences being seen in the amygdala and ventral striatum even if only incorrect trials were considered. The results indicate that a network of frontolimbic regions may provide emotional bias signals during facial recognition. Hum Brain Mapp, 2009. © 2009 Wiley‐Liss, Inc.     

Sustained happiness? Lack of repetition suppression in right-ventral visual cortex for happy faces

Emotional stimuli have been shown to preferentially engage initial attention but their sustained effects on neural processing remain largely unknown. The present study evaluated whether emotional faces engage sustained neural processing by examining the attenuation of neural repetition suppression to repeated emotional faces. Repetition suppression of neural function refers to the general reduction of neural activity when processing a repeated stimulus. Preferential processing of emotional face stimuli, however, should elicit sustained neural processing such that repetition suppression to repeated emotional faces is attenuated relative to faces with no emotional content. We measured the reduction of functional magnetic resonance imaging signals associated with immediate repetition of neutral, angry and happy faces. Whereas neutral faces elicited the greatest suppression in ventral visual cortex, followed by angry faces, repetition suppression was the most attenuated for happy faces. Indeed, happy faces showed almost no repetition suppression in part of the right-inferior occipital and fusiform gyri, which play an important role in face-identity processing. Our findings suggest that happy faces are associated with sustained visual encoding of face identity and thereby assist in the formation of more elaborate representations of the faces, congruent with findings in the behavioral literature.     

Spatiotemporal dynamics in human visual cortex rapidly encode the emotional content of faces

Recognizing emotion in faces is important in human interaction and survival, yet existing studies do not paint a consistent picture of the neural representation supporting this task. To address this, we collected magnetoencephalography (MEG) data while participants passively viewed happy, angry and neutral faces. Using time‐resolved decoding of sensor‐level data, we show that responses to angry faces can be discriminated from happy and neutral faces as early as 90 ms after stimulus onset and only 10 ms later than faces can be discriminated from scrambled stimuli, even in the absence of differences in evoked responses. Time‐resolved relevance patterns in source space track expression‐related information from the visual cortex (100 ms) to higher‐level temporal and frontal areas (200–500 ms). Together, our results point to a system optimised for rapid processing of emotional faces and preferentially tuned to threat, consistent with the important evolutionary role that such a system must have played in the development of human social interactions.     

Common and distinct brain activation to threat and safety signals in social phobia

BACKGROUND: Little is known about the functional neuroanatomy underlying the processing of emotional stimuli in social phobia. OBJECTIVES: To investigate specific brain activation that is associated with the processing of threat and safety signals in social phobics. METHODS: Using functional magnetic resonance imaging, brain activation was measured in social phobic and nonphobic subjects during the presentation of angry, happy and neutral facial expressions under free viewing conditions. RESULTS: Compared to controls, phobics showed increased activation of extrastriate visual cortex regardless of facial expression. Angry, but not neutral or happy, faces elicited greater insula responses in phobics. In contrast, both angry and happy faces led to increased amygdala activation in phobics. CONCLUSIONS: The results support the hypothesis that the amygdala is involved in the processing of negative and positive stimuli. Furthermore, social phobics respond sensitively not only to threatening but also to accepting faces and common and distinct neural mechanisms appear to be associated with the processing of threat versus safety signals.     

Affective neural circuitry during facial emotion processing in pediatric bipolar disorder.

BACKGROUND: Facial emotions are central to human interaction. Identifying pathophysiology in affect processing circuitry that supports the ability to assess facial emotions might facilitate understanding of affect regulation in pediatric bipolar disorder. METHODS: Ten euthymic, unmedicated pediatric bipolar patients and 10 healthy control subjects matched for age, gender, race, socioeconomic status, and IQ were scanned with functional magnetic resonance imaging. Angry, happy, and neutral faces were presented in 30-sec blocks, with a 20-sec rest period between blocks. Subjects were asked to press a button when each face appeared, to ensure that attention was maintained on-task. RESULTS: In bipolar patients, in response to both angry and happy faces relative to neutral faces, we observed reduced activation of right rostral ventrolateral prefrontal cortex together with increased activity in right pregenual anterior cingulate, amygdala, and paralimbic cortex. Bipolar patients also showed reduced activation of visual areas in occipital cortex together with greater activation in higher-order visual perceptual areas, including superior temporal sulcus and fusiform gyrus with angry faces and posterior parietal cortex with happy faces. CONCLUSIONS: Findings document a disturbance in affective neurocircuitry in pediatric bipolar disorder. Reduced activation in ventrolateral prefrontal cortex might reflect diminished top-down control that leads to the observed exaggerated activation in amygdala and paralimbic areas. Changes in occipital areas might represent an effort to gate sensory input when affective responses to the faces could not be successfully modulated. Disturbances in affect processing circuitry could contribute to emotional dysregulation and social cognitive difficulties in bipolar youth.     

Dopamine boosts memory for angry faces in Parkinson's disease

The influence of emotional context on cognitive operations is of fundamental importance for the evolution of higher cognitive functions and their disturbance in neuropsychiatric disorders. The dopamine pathways projecting to prefrontal cortex and the basal ganglia are assumed to play a major role in such emotion‐cognition interactions. Here we provide evidence for such a role by studying working memory for emotional faces in patients with Parkinson's Disease. We studied 25 patients with Parkinson's disease during their on and off medication states. Faces with emotional expressions (happy, angry, sad, neutral or fearful) were shown and the participants had to remember and later recall the identity of the faces ignoring the expressions. We found that dopaminergic medication enhances working memory for angry faces and suppresses it for sad faces. The results elucidate neurochemical mechanisms for the saliency of threatening information and support cognitive explanations of the antidepressant effects of dopamine. They also suggest a role for dopamine in changing emotional‐cognitive biases rather than as a generic cognitive enhancer. © 2010 Movement Disorder Society.     

Prediction errors to emotional expressions: the roles of the amygdala in social referencing

Social referencing paradigms in humans and observational learning paradigms in animals suggest that emotional expressions are important for communicating valence. It has been proposed that these expressions initiate stimulus-reinforcement learning. Relatively little is known about the role of emotional expressions in reinforcement learning, particularly in the context of social referencing. In this study, we examined object valence learning in the context of a social referencing paradigm. Participants viewed objects and faces that turned toward the objects and displayed a fearful, happy or neutral reaction to them, while judging the gender of these faces. Notably, amygdala activation was larger when the expressions following an object were less expected. Moreover, when asked, participants were both more likely to want to approach, and showed stronger amygdala responses to, objects associated with happy relative to objects associated with fearful expressions. This suggests that the amygdala plays two roles in social referencing: (i) initiating learning regarding the valence of an object as a function of prediction errors to expressions displayed toward this object and (ii) orchestrating an emotional response to the object when value judgments are being made regarding this object.     

Time-varying amygdala response to emotional faces in generalized social phobia.

BACKGROUND: Individuals with social phobia (SP) have altered behavioral and neural responses to emotional faces and are hypothesized to have deficits in inhibiting emotion-related amygdala responses. We tested for such amygdala deficits to emotional faces in a sample of individuals with SP. METHOD: We used functional magnetic resonance imaging (fMRI) to examine the neural substrates of emotional face processing in 14 generalized SP (gSP) and 14 healthy comparison (HC) participants. Analyses focused on the temporal dynamics of the amygdala, prefrontal cortex (PFC), and fusiform face area (FFA) across blocks of neutral, fear, contempt, anger, and happy faces in gSP versus HC participants. RESULTS: Amygdala responses in participants with gSP occurred later than the HC participants to fear, angry, and happy faces. Parallel PFC responses were found for happy and fear faces. There were no group differences in temporal response patterns in the FFA. CONCLUSIONS: This finding might reflect a neural correlate of atypical orienting responses among individuals with gSP. Commonly reported SP deficits in habituation might reflect neural regions associated with emotional self-evaluations rather than the amygdala. This study highlights the importance of considering time-varying modulation when examining emotion-related processing in individuals with gSP.     

Amygdala hyperactivation to angry faces in intermittent explosive disorder

BackgroundIndividuals with intermittent explosive disorder (IED) were previously found to exhibit amygdala hyperactivation and relatively reduced orbital medial prefrontal cortex (OMPFC) activation to angry faces while performing an implicit emotion information processing task during functional magnetic resonance imaging (fMRI). This study examines the neural substrates associated with explicit encoding of facial emotions among individuals with IED.MethodTwenty unmedicated IED subjects and twenty healthy, matched comparison subjects (HC) underwent fMRI while viewing blocks of angry, happy, and neutral faces and identifying the emotional valence of each face (positive, negative or neutral). We compared amygdala and OMPFC reactivity to faces between IED and HC subjects. We also examined the relationship between amygdala/OMPFC activation and aggression severity.ResultsCompared to controls, the IED group exhibited greater amygdala response to angry (vs. neutral) facial expressions. In contrast, IED and control groups did not differ in OMPFC activation to angry faces. Across subjects amygdala activation to angry faces was correlated with number of prior aggressive acts.ConclusionsThese findings extend previous evidence of amygdala dysfunction in response to the identification of an ecologically-valid social threat signal (processing angry faces) among individuals with IED, further substantiating a link between amygdala hyperactivity to social signals of direct threat and aggression.     

Neural responses to emotional and neutral facial expressions in chronically violent men

Background

Abnormal neural responses to others’ emotions, particularly cues of threat and distress, have been implicated in the development of chronic violence. We examined neural responses to several emotional cues within a prospectively identified group of chronically violent men. We also explored the association between neural responses to social emotions and psychopathic features.

Methods

We compared neural responses to happy, sad, angry, fearful and neutral faces between chronically violent (n = 22) and non-violent (n = 20) men using functional magnetic resonance imaging (fMRI). Participants were prospectively identified from a longitudinal study based on information collected from age 7 to 27 years. We assessed psychopathic features using a self-report measure administered in adulthood.

Results

The chronically violent men exhibited significantly reduced neural responses in the dorsomedial prefrontal cortex to all faces, regardless of the emotional content, compared with nonviolent men. We also observed a hyperactive amygdala response to neutral faces in chronically violent men, but only within the context of viewing happy faces. Moreover, they exhibited a greater dorsomedial prefrontal cortex response to mildly fearful faces than nonviolent men. These abnormalities were not associated with psychopathic features in chronically violent men.

Limitations

It remains unclear whether the observed neural abnormalities preceded or are a consequence of persistent violence, and these results may not generalize to chronically violent women.

Conclusion

Chronically violent men exhibit a reduced neural response to facial cues regardless of emotional content. It appears that chronically violent men may view emotionally ambiguous facial cues as potentially threatening and implicitly reinterpret subtle cues of fear in others so they no longer elicit a negative response.     

Neural responses to emotional stimuli are associated with childhood family stress.

BACKGROUND: An early family environment marked by harsh parenting has been related to risk for multiple mental disorders in adulthood, risks that may be mediated, in part, by deficits in emotion regulation skills. This study examined neural mechanisms underlying these consequences of "risky" families (RF) by exploring neural activity to tasks involving responses to emotional stimuli. METHODS: Participants completed an assessment of RF and participated in a functional magnetic resonance imaging (fMRI) investigation that examined 1) amygdala reactivity to observation of fearful/angry faces; 2) amygdala and right ventrolateral prefrontal cortex (RVLPFC) reactivity to labeling emotions displayed in these faces; and 3) the relation between RVLPFC and amygdala activity during the labeling task. RESULTS: Offspring from nonrisky families showed expected amygdala reactivity to observing fearful/angry faces and expected activation of RVLPFC while labeling the emotions, which was significantly negatively correlated (-.44) with amygdala activation. Offspring from risky families showed little amygdala activation during the observation task and a strong positive correlation (+.66) between RVLPFC and amygdala activation in the labeling task, suggesting a possible dysregulation in the neural systems involved in responses to emotional stimuli. CONCLUSIONS: Offspring from risky families exhibit atypical responses to emotional stimuli that are evident at the neural level.     

Prefrontal cortical response to emotional faces in individuals with major depressive disorder in remission

Abnormalities in the response of the orbitofrontal cortex (OFC) and dorsolateral prefrontal cortex (DLPFC) to negative emotional stimuli have been reported in acutely depressed patients. However, there is a paucity of studies conducted in unmedicated individuals with major depressive disorder in remission (rMDD) to assess whether these are trait abnormalities. To address this issue, 19 medication-free rMDD individuals and 20 healthy comparison (HC) participants were scanned using functional magnetic resonance imaging while performing an implicit emotion processing task in which they labeled the gender of faces depicting negative (fearful), positive (happy) and neutral facial expressions. The rMDD and HC groups were compared using a region-of-interest approach for two contrasts: fear vs. neutral and happy vs. neutral. Relative to HC, rMDD showed reduced activation in left OFC and DLPFC to fearful (vs. neutral) faces. Right DLPFC activation to fearful (vs. neutral) faces in the rMDD group showed a significant positive correlation with duration of euthymia. The findings support deficits in left OFC and DLPFC responses to negative emotional stimuli during euthymic periods of MDD, which may reflect trait markers of the illness or a 'scar' due to previous depression. Recovery may also be associated with compensatory increases in right DLPFC functioning.     

Effects of gaze direction,head orientation and valence of facial expression on amygdala activity

There is increasing evidence for a role of the amygdala in processing gaze direction and emotional relevance of faces. In this event-related functional magnetic resonance study we investigated amygdala responses while we orthogonally manipulated head direction, gaze direction and facial expression (angry, happy and neutral). This allowed us to investigate effects of stimulus ambiguity, low-level factors and non-emotional factors on amygdala activation. Averted vs direct gaze induced increased activation in the right dorsal amygdala regardless of facial expression and head orientation. Furthermore, valence effects were found in the ventral amygdala and strongly dependent on head orientation. We observed enhanced activation to angry and neutral vs happy faces for observer-directed faces in the left ventral amygdala while the averted head condition reversed this pattern resulting in increased activation to happy as compared to angry and neutral faces. These results suggest that gaze direction drives specifically dorsal amygdala activation regardless of facial expression, low-level perceptual factors or stimulus ambiguity. The role of the amygdala is thus not restricted to the detection of potential threat, but has a more general role in attention processes. Furthermore, valence effects are associated with activation of the ventral amygdala and strongly influenced by non-emotional factors.     

Shyness and the first 100 ms of emotional face processing

Although shyness is presumed to be related to an increased sensitivity to detect motivationally salient social stimuli, we know little of how shyness affects the early perception of facial emotions. We demonstrate here that individual differences in normative shyness were related to brain responses to some emotional faces as early as the P1 electrocortical component, 80-130 ms after stimulus onset. High-shy individuals showed reduced P1 amplitude for fearful faces compared to neutral faces. Low-shy individuals processed happy faces faster than other emotions and showed increased P1 amplitudes for happy faces over neutral faces. Regardless of shyness level, participants showed increased amplitudes in the N170 component (130-200 ms) for all emotions over neutral conditions, particularly for the emotion of fear. This study presents the first evidence that shyness is related to early electrocortical responses to the processing of fearful faces, consistent with a fast-path amygdala sensitivity model.