Enhanced occipital and anterior cingulate activation in men but not in women during exposure to angry and fearful male faces

Blood-oxygenation-level-dependent signal was measured with functional magnetic resonance imaging in 24 healthy young subjects (12 men and 12 women) during viewing of angry, fearful, and neutral male and female face pictures. Exposure to angry male as opposed to angry female faces activated the visual cortex and the anterior cingulate gyrus significantly more in men than in women. A similar sex-differential brain activation pattern was present during exposure to fearful but not neutral faces. Previous behavioral studies indicate enhanced physiological arousal in men but not in women during exposure to angry male as opposed to female faces, and brain imaging studies have shown that the occipital cortex and the anterior cingulate gyrus are influenced by activity in the autonomic nervous system as well as by visual attention. Hence, we suggest that the elevated occipital and anterior cingulate activation in men during confrontation with other angry and fearful males may reflect enhanced vigilance in a potentially dangerous situation.     

厌恶与恐惧面孔的记忆编码、保持、提取

情绪记忆增强效应在负性情绪记忆研究中被反复证实。尽管厌恶和恐惧同属负性情绪, 提示威胁的存在, 但由于它们的进化意义和生理功能不同, 可能导致它们对记忆的编码、保持、提取三个阶段不同的调节方向或调节强度。本文采用延迟再认任务, 采用事件相关电位考察健康成年被试对唤醒度和效价相当的恐惧和厌恶面孔的记忆编码、保持和提取。结果显示, 1)在记忆编码的早期, 被试主要加强了对恐惧面孔的注意(P1)和结构编码(N170), 而厌恶信息的加工受到了抑制; 2)从记忆编码晚期到记忆保持的整个阶段, 被试对厌恶信息的精细评估(编码阶段P3)和复述保持(保持阶段的负走向慢波)均强于恐惧信息; 3)相比于恐惧面孔, 厌恶面孔可能在工作记忆系统形成了更强的表征, 从而使被试在记忆提取时可回忆起更多的细节, 对记忆提取的信心更足(提取阶段P3)。这后两条发现是导致行为层面上厌恶情绪记忆优于恐惧情绪记忆的原因。本研究为“厌恶比恐惧具有更强的记忆增强效应”提供了高时间分辨率的脑活动层面的证据, 从而进一步揭示了负性情绪增强记忆的认知机制。     

The influence of indirect and direct emotional processing on memory for facial expressions

We used the remember-know procedure (Tulving, 1985 ) to test the behavioural expression of memory following indirect and direct forms of emotional processing at encoding. Participants (N=32) viewed a series of facial expressions (happy, fearful, angry, and neutral) while performing tasks involving either indirect (gender discrimination) or direct (emotion discrimination) emotion processing. After a delay, participants completed a surprise recognition memory test. Our results revealed that indirect encoding of emotion produced enhanced memory for fearful faces whereas direct encoding of emotion produced enhanced memory for angry faces. In contrast, happy faces were better remembered than neutral faces after both indirect and direct encoding tasks. These findings suggest that fearful and angry faces benefit from a recollective advantage when they are encoded in a way that is consistent with the predictive nature of their threat. We propose that the broad memory advantage for happy faces may reflect a form of cognitive flexibility that is specific to positive emotions.     

Fearful expressions enhance recognition memory: electrophysiological evidence

Facial expressions play a key role in affective and social behavior. However, the temporal dynamics of the brain responses to emotional faces remain still unclear, in particular an open question is at what stage of face processing expressions might influence encoding and recognition memory. To try and answer this question we recorded the event-related potentials (ERPs) elicited in an old/new recognition task. A novel aspect of the present design was that whereas faces were presented during the study phase with either a happy, fearful or neutral expression, they were always neutral during the memory retrieval task. The ERP results showed three main findings: An enhanced early fronto-central positivity for faces encoded as fearful, both during the study and the retrieval phase. During encoding subsequent memory (Dm effect) was influenced by emotion. At retrieval the early components P100 and N170 were modulated by the emotional expression of the face at the encoding phase. Finally, the later ERP components related to recognition memory were modulated by the previously encoded facial expressions. Overall, these results suggest that face recognition is modulated by top-down influences from brain areas associated with emotional memory, enhancing encoding and retrieval in particular for fearful emotional expressions.     

Links between rapid ERP responses to fearful faces and conscious awareness

To study links between rapid ERP responses to fearful faces and conscious awareness, a backward‐masking paradigm was employed where fearful or neutral target faces were presented for different durations and were followed by a neutral face mask. Participants had to report target face expression on each trial. When masked faces were clearly visible (200 ms duration), an early frontal positivity, a later more broadly distributed positivity, and a temporo‐occipital negativity were elicited by fearful relative to neutral faces, confirming findings from previous studies with unmasked faces. These emotion‐specific effects were also triggered when masked faces were presented for only 17 ms, but only on trials where fearful faces were successfully detected. When masked faces were shown for 50 ms, a smaller but reliable frontal positivity was also elicited by undetected fearful faces. These results demonstrate that early ERP responses to fearful faces are linked to observers' subjective conscious awareness of such faces, as reflected by their perceptual reports. They suggest that frontal brain regions involved in the construction of conscious representations of facial expression are activated at very short latencies.     

Dissociation of the neural systems for working memory maintenance of verbal and nonspatial visual information

Working memory for names and faces was investigated to ascertain whether verbal and nonspatial visual information is maintained in working memory by separate neural systems. The subjects performed a delayed match-to-sample task for famous or unfamous faces and names and a sensorimotor control task. Several occipital, temporal, parietal, and prefrontal areas were activated during all memory delays, in comparison with the control delays. Greater delay activity for unfamous faces than for names was obtained in the right fusiform gyrus, right inferior frontal gyrus (IFG), right IFG/ precentral gyrus, and right medial superior frontal gyrus, whereas greater delay activity for unfamous names than for faces was observed in the precuneus, left insula/postcentral gyrus, and left IFG/ precentral gyrus. There was no significant difference in the prefrontal activity in the comparison between famous faces and names. Greater delay activity for famous names than for faces was obtained in visual association and parietal areas. The results indicate that there is a functional dissociation based on information type within the neural system that is responsible for working memory maintenance of verbal and nonspatial visual information.     

The amygdala is involved in affective priming effect for fearful faces

The object of this study was to investigate whether the amygdala is involved in affective priming effect after stimuli are encoded unconsciously and consciously. During the encoding phase, each masked face (fearful or neutral) was presented to participants six times for 17ms each, using a backward masking paradigm. During the retrieval phase, participants made a fearful/neutral judgment for each face. Half of the faces had the same valence as that seen during encoding (congruent condition) and the other half did not (incongruent condition). Participants were divided into unaware and aware groups based on their subjective and objective awareness assessments. The fMRI results showed that during encoding, the amygdala elicited stronger activation for fearful faces than neutral faces but differed in the hemisphere according to the awareness level. During retrieval, the amygdala showed a significant repetition priming effect, with the congruent faces producing less activation than the incongruent faces, especially for fearful faces. These data suggest that the amygdala is important in unconscious retrieving of memories for emotional faces whether they are encoded consciously or unconsciously.     

“Wanted!” The effects of reward on face recognition: electrophysiological correlates

The aim of the present study was to uncover the temporal dynamics of face recognition as a function of reward. Event-related potentials (ERPs) were recorded during the encoding and the subsequent old/new memory test in response to faces that could be associated with a monetary reward. The behavioral results showed that faces associated with reward at both encoding and retrieval were recognized better than the unrewarded ones. ERP responses highlighted that successful encoding predictive of subsequent memory was greater for faces associated with reward than for faces without reward-driven motivational learning. At retrieval, an early positive-going component was elicited for potentially rewarded faces on frontal regions, while the occipito-temporal N170 component showed priming effects as a function of reward. Later on, larger centro-parietal ERP components, related to recognition memory, were found selectively for reward-associated faces. Remarkably, electrophysiological responses varied in a graded manner, with the largest amplitude yielded by faces with double reward, followed by faces associated with reward only at encoding. Taken together, the present data show that the processing of outcome expectations affects face structural encoding and increases memory efficiency, yielding a robust and sustained modulation over frontal and temporal areas where reward and memory mechanisms operate in conjunction.     

Coarse threat images reveal theta oscillations in the amygdala: A magnetoencephalography study

Neurocognitive models propose a specialized neural system for processing threat-related information, in which the amygdala plays a key role in the analysis of threat cues. fMRI research indicates that the amygdala is sensitive to coarse visual threat relevant information—for example, low spatial frequency (LSF) fearful faces. However, fMRI cannot determine the temporal or spectral characteristics of neural responses. Consequently, we used magnetoencephalography to explore spatiotemporal patterns of activity in the amygdala and cortical regions with blurry (LSF) and normal angry, fearful, and neutral faces. Results demonstrated differences in amygdala activity between LSF threat-related and LSF neutral faces (50–250 msec after face onset). These differences were evident in the theta range (4–8 Hz) and were accompanied by power changes within visual and frontal regions. Our results support the view that the amygdala is involved in the early processing of coarse threat related information and that theta is important in integrating activity within emotion-processing networks.     

Individual differences in cardiac vagal tone are associated with differential neural responses to facial expressions at different spatial frequencies: An ERP and sLORETA study

A previous study has shown that greater cardiac vagal tone, reflecting effective self-regulatory capacity, was correlated with superior visual discrimination of fearful faces at high spatial frequency Park et al. (Biological Psychology 90:171?C178, 2012b). The present study investigated whether individual differences in cardiac vagal tone (indexed by heart rate variability) were associated with different event-related brain potentials (ERPs) in response to fearful and neutral faces. Thirty-six healthy participants discriminated the emotion of fearful and neutral faces at broad, high, and low spatial frequencies, while ERPs were recorded. Participants with low resting heart rate variability??characterized by poor functioning of regulatory systems??exhibited significantly greater N200 activity in response to fearful faces at low spatial frequency and greater LPP responses to neutral faces at high spatial frequency. Source analyses??estimated by standardized low-resolution brain electromagnetic tomography (sLORETA)??tended to show that participants with low resting heart rate variability exhibited increased source activity in visual areas, such as the cuneus and the middle occipital gyrus, as compared with participants with high resting heart rate variability. The hyperactive neural activity associated with low cardiac vagal tone may account for hypervigilant response patterns and emotional dysregulation, which heightens the risk of developing physical and emotional problems.     

Emotional memories are not all created equal: evidence for selective memory enhancement

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.     

Residual effects of emotion are reflected in enhanced visual activity after sleep

Research has investigated how sleep affects emotional memory and how emotion enhances visual processing, but these questions are typically asked by re-presenting an emotional stimulus at retrieval. For the first time, we investigate whether sleep affects neural activity during retrieval when the memory cue is a neutral context that was previously presented with either emotional or nonemotional content during encoding. Participants encoded scenes composed of a negative or neutral object on a neutral background either in the morning (preceding 12 hours awake; wake group) or evening (preceding 12 hours including a night of sleep; sleep group). At retrieval, participants viewed the backgrounds without their objects, distinguishing new backgrounds from those previously studied. Occipital activity was greater within the sleep group than the wake group specifically during the successful retrieval of neutral backgrounds that had been studied with negative (but not neutral) objects. Moreover, there was enhanced connectivity between the middle occipital gyrus and hippocampus following sleep. Within the sleep group, the percentage of REM sleep obtained correlated with activity in the middle occipital gyrus, lingual gyrus, and cuneus during the successful retrieval of neutral backgrounds previously paired with negative objects. These results confirm that emotion affects neural activity during retrieval even when the cues themselves are neutral, and demonstrate, for the first time, that this residual effect of emotion on visual activity is greater after sleep and may be maximized by REM sleep.     

Age-related neural activity during allocentric spatial memory

Age-related decline in allocentric (viewer-independent) spatial memory is seen across species. We employed a virtual reality analogue of the Morris Water Maze to study the effect of healthy ageing on neural activity during allocentric spatial memory using functional magnetic resonance imaging. Voxel-based morphometry was used to ascertain hippocampal volumetric integrity. A widespread neural network comprising frontal, parietal, occipital, thalamic, and cerebellar regions was activated in young and older adults, but only young adults significantly activated bilateral hippocampus and left parahippocampus, as well as right frontal pole and dorso-lateral prefrontal cortex (DLPFC) during encoding and right DLPC during retrieval. Hippocampal grey matter volume was unchanged in older adults; however, prefrontal and parahippocampal functional attenuation was accompanied by volumetric reduction. We conclude that the decline in allocentric spatial memory with age is associated with attenuated hippocampal function, as well as compromised function and structure of prefrontal and parahippocampal regions.     

Women's own-gender bias in face recognition memory

Women remember more female than male faces, whereas men do not seem to display an own-gender bias in face recognition memory. Why women remember female faces to a greater extent than male faces is unclear; one proposition is that women attend more to and thereby process female faces more effortfully than male faces during encoding. A manipulation that distracts attention and reduces effortful processing may therefore decrease women's own-gender bias by reducing memory for female faces relative to male faces. In three separate experiments, women and men encoded female and male faces for later recognition in full attention and divided attention conditions. Results consistently showed that women, in contrast to men, displayed a reliable own-gender bias. Importantly, the magnitude of women's own-gender bias was not reduced in divided attention conditions, indicating that it is not a result of effortful processing of female faces. We suggest these results reflect that women have greater perceptual expertise for female faces, facilitating recognition memory.     

The development of emotional face and eye gaze processing

Recent research has demonstrated that infants' attention towards novel objects is affected by an adult's emotional expression and eye gaze toward the object. The current event-related potential (ERP) study investigated how infants at 3, 6, and 9 months of age process fearful compared to neutral faces looking toward objects or averting gaze away from objects. Furthermore, we examined how the processing of novel objects is affected by gaze direction and emotional expression. We hypothesized that an adult's fearful expression should be particularly salient when it is directed toward a referent in the environment. Furthermore, responses to objects should be increased if the face previously expressed fear toward the object. Three-month-olds did not show differential neural responses to fearful vs. neutral faces regardless of gaze direction. Six-month-olds showed an enhanced negative central (Nc) component for fearful relative to neutral faces looking toward objects, but not when eye gaze was averted away from the objects. Furthermore, 6-month-olds showed an enhanced Nc for objects that had been gaze-cued by a fearful compared to a neutral face. Nine-month-olds showed an enhanced Nc for fearful relative to neutral faces in both eye gaze conditions and showed an enhanced Nc for objects that had been gaze-cued by a neutral face. The findings are discussed in the context of social cognitive and brain development.     

Functional brain activation to emotional and nonemotional faces in healthy children: Evidence for developmentally undifferentiated amygdala function during the school-age period

The amygdala is a key region in emotion processing. In particular, fMRI studies have demonstrated that the amygdala is active during the viewing of emotional faces. Previous research has consistently found greater amygdala responses to fearful than to neutral faces in adults, convergent with a focus in the animal literature on the amygdala’s role in fear processing. Studies have shown that the amygdala also responds differentially to other facial emotion types in adults. Yet the literature regarding when this differential amygdala responsivity develops is limited and mixed. Thus, the goal of the present study was to examine amygdala responses to emotional and neutral faces in a relatively large sample of healthy school-age children (N?=?52). Although the amygdala was active in response to emotional and neutral faces, the results did not support the hypothesis that the amygdala responds differentially to emotional faces in 7- to 12-year-old children. Nonetheless, amygdala activity was correlated with the severity of subclinical depression symptoms and with emotional regulation skills. Additionally, sex differences were observed in frontal, temporal, and visual regions, as well as effects of pubertal development in visual regions. These findings suggest important differences in amygdala reactivity in childhood.     

Neural substrates for episodic encoding and recognition of unfamiliar faces

Functional MRI was used to investigate brain activation in healthy volunteers during encoding of unfamiliar faces as well as during correct recognition of newly learned faces (CR) compared to correct identification of distractor faces (CF), missed alarms (not recognizing previously presented faces, MA), and false alarms (incorrectly recognizing newly presented faces, FA). Encoding was associated with frontal, occipital/fusiform, thalamic, and cerebellar activation. CR produced activation in frontal and cerebellar regions, whereas CF activated frontal and occipitotemporal regions as well as the thalamus. In contrast, MA was associated with frontal and thalamic activation, and FA with frontal activation. The CR minus CF comparison showed left lateral prefrontal and parietal activation, while no suprathreshold positive signal changes were detected when subtracting the other conditions (CR minus MA, CR minus FA, and vice versa). These results support the view that the successful episodic retrieval of newly learned faces is based on a dorsal visual stream mechanism.     

Effects of aging on the neural correlates of successful item and source memory encoding

To investigate the neural basis of age-related source memory (SM) deficits, young and older adults were scanned with fMRI while encoding faces, scenes, and face-scene pairs. Successful encoding activity was identified by comparing encoding activity for subsequently remembered versus forgotten items or pairs. Age deficits in successful encoding activity in hippocampal and prefrontal regions were more pronounced for SM (pairs) as compared with item memory (faces and scenes). Age-related reductions were also found in regions specialized in processing faces (fusiform face area) and scenes (parahippocampal place area), but these reductions were similar for item and SM. Functional connectivity between the hippocampus and the rest of the brain was also affected by aging; whereas connections with posterior cortices were weaker in older adults, connections with anterior cortices, including prefrontal regions, were stronger in older adults. Taken together, the results provide a link between SM deficits in older adults and reduced recruitment of hippocampal and prefrontal regions during encoding. The functional connectivity findings are consistent with a posterior-anterior shift with aging previously reported in several cognitive domains and linked to functional compensation.     

Goal-relevant situations facilitate memory of neutral faces

Emotional situations are typically better remembered than neutral situations, but the psychological conditions and brain mechanisms underlying this effect remain debated. Stimulus valence and affective arousal have been suggested to explain the major role of emotional stimuli in memory facilitation. However, neither valence nor arousal are sufficient affective dimensions to explain the effect of memory facilitation. Several studies showed that negative and positive details are better remembered than neutral details. However, other studies showed that neutral information encoded and coupled with arousal did not result in a memory advantage compared with neutral information not coupled with arousal. Therefore, we suggest that the fundamental affective dimension responsible for memory facilitation is goal relevance. To test this hypothesis at behavioral and neural levels, we conducted a functional magnetic resonance imaging study and used neutral faces embedded in goal-relevant or goal-irrelevant daily life situations. At the behavioral level, we found that neutral faces encountered in goal-relevant situations were better remembered than those encountered in goal-irrelevant situations. To explain this effect, we studied neural activations involved in goal-relevant processing at encoding and in subsequent neutral face recognition. At encoding, activation of emotional brain regions (anterior cingulate, ventral striatum, ventral tegmental area, and substantia nigra) was greater for processing of goal-relevant situations than for processing of goal-irrelevant situations. At the recognition phase, despite the presentation of neutral faces, brain activation involved in social processing (superior temporal sulcus) to successfully remember identities was greater for previously encountered faces in goal-relevant than in goal-irrelevant situations.     

A tale of two negatives: differential memory modulation by threat-related facial expressions

Facial expressions serve as cues that encourage viewers to learn about their immediate environment. In studies assessing the influence of emotional cues on behavior, fearful and angry faces are often combined into one category, such as "threat-related," because they share similar emotional valence and arousal properties. However, these expressions convey different information to the viewer. Fearful faces indicate the increased probability of a threat, whereas angry expressions embody a certain and direct threat. This conceptualization predicts that a fearful face should facilitate processing of the environment to gather information to disambiguate the threat. Here, we tested whether fearful faces facilitated processing of neutral information presented in close temporal proximity to the faces. In Experiment 1, we demonstrated that, compared with neutral faces, fearful faces enhanced memory for neutral words presented in the experimental context, whereas angry faces did not. In Experiment 2, we directly compared the effects of fearful and angry faces on subsequent memory for emotional faces versus neutral words. We replicated the findings of Experiment 1 and extended them by showing that participants remembered more faces from the angry face condition relative to the fear condition, consistent with the notion that anger differs from fear in that it directs attention toward the angry individual. Because these effects cannot be attributed to differences in arousal or valence processing, we suggest they are best understood in terms of differences in the predictive information conveyed by fearful and angry facial expressions.