fMRI of fearful facial affect recognition in panic disorder: the cingulate gyrus-amygdala connection

BACKGROUND: This study investigated cingulate cortex (CC) and amygdala response to fearful facial affect recognition in patients with panic disorder (PD) as measured by BOLD fMRI during the presentation of static facial images. METHODS: Eight patients with PD and eight controls were studied. Scanning was performed on a GE Signa 1.5-T scanner. Echo planar and high-resolution MR images were acquired. RESULTS: Controls produced greater CC activation compared to patients with PD in response to fearful faces. Furthermore, patients with PD produced less amygdala activation than controls in response to fearful faces. During the neutral face condition, overall activation for the CC was significantly greater in PD patients although anterior cingulate cortex (ACC) activation was not as markedly different between both groups. There were no between group differences in amygdala activation on exposure to the neutral face. Only left CC activation was significantly correlated negatively with HAM-A in PD patients in the fearful facial affect condition. LIMITATIONS: Although comparable to similar studies, the sample size is small enough to warrant further investigation. Also, the effects of medication need to be considered when interpreting these results. CONCLUSIONS: Patients with PD activate the ACC and amygdala significantly less than controls when asked to identify fearful facial affect during fMRI. The higher the anxiety, the lower the left CC activation. Thus, chronic hyperarousal in PD may diminish attentional resources and emotional response reflected in reduced ACC and amygdala activation. Even if these are medication effects, the differences from controls are clinically relevant.     

Neural responses to facial expression and face identity in the monkey amygdala

The amygdala is purported to play an important role in face processing, yet the specificity of its activation to face stimuli and the relative contribution of identity and expression to its activation are unknown. In the current study, neural activity in the amygdala was recorded as monkeys passively viewed images of monkey faces, human faces, and objects on a computer monitor. Comparable proportions of neurons responded selectively to images from each category. Neural responses to monkey faces were further examined to determine whether face identity or facial expression drove the face-selective responses. The majority of these neurons (64%) responded both to identity and facial expression, suggesting that these parameters are processed jointly in the amygdala. Large fractions of neurons, however, showed pure identity-selective or expression-selective responses. Neurons were selective for a particular facial expression by either increasing or decreasing their firing rate compared with the firing rates elicited by the other expressions. Responses to appeasing faces were often marked by significant decreases of firing rates, whereas responses to threatening faces were strongly associated with increased firing rate. Thus global activation in the amygdala might be larger to threatening faces than to neutral or appeasing faces.     

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

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

Response properties of the human fusiform face area

We used functional magnetic resonance imaging to study the response properties of the human fusiform face area (FFA: Kanwisher, McDermott, & Chun, 1997) to a variety of face-like stimuli in order to clarify the functional role of this region. FFA responses were found to be (1) equally strong for cat, cartoon and human faces despite very different image properties, (2) equally strong for entire human faces and faces with eyes occluded but weaker for eyes shown alone, (3) equal for front and profile views of human heads, but declining in strength as faces rotated away from view, and (4) weakest for nonface objects and houses. These results indicate that generalisation of the FFA response across very different face types cannot be explained in terms of a specific response to a salient facial feature such as the eyes or a more general response to heads. Instead, the FFA appears to be optimally tuned to the broad category of faces.     

RESPONSE PROPERTIES OF THE HUMAN FUSIFORM FACE AREA

We used functional magnetic resonance imaging to study the response properties of the human fusiform face area (FFA: Kanwisher, McDermott, & Chun, 1997) to a variety of face-like stimuli in order to clarify the functional role of this region. FFA responses were found to be (1) equally strong for cat, cartoon and human faces despite very different image properties, (2) equally strong for entire human faces and faces with eyes occluded but weaker for eyes shown alone, (3) equal for front and profile views of human heads, but declining in strength as faces rotated away from view, and (4) weakest for nonface objects and houses. These results indicate that generalisation of the FFA response across very different face types cannot be explained in terms of a specific response to a salient facial feature such as the eyes or a more general response to heads. Instead, the FFA appears to be optimally tuned to the broad category of faces.     

Neural correlates to seen gaze-direction and head orientation in the macaque monkey amygdala

Human neuropsychological studies suggest that the amygdala is implicated in social cognition, in which cognition of seen gaze-direction, especially the direct gaze, is essential, and that the perception of gaze direction is modulated by the head orientation of the facial stimuli. However, neural correlates to these issues remain unknown. In the present study, neuronal activity was recorded from the macaque monkey amygdala during performance of a sequential delayed non-matching-to-sample task based on gaze direction. The facial stimuli consisted of two head orientations (frontal; straight to the monkey, profile; 30 degrees rightwards from the front) with different gaze directions (directed toward and averted to the left or right of the monkey). Of the 1091 neurons recorded, 61 responded to more than one facial stimulus. Of these face-responsive neurons, 44 displayed responses selective to the facial stimuli (face neurons). Most amygdalar face neurons discriminated both gaze direction and head orientation, and exhibited a significant interaction between the two types about information. Furthermore, factor analysis on the response magnitudes of the face neurons to the facial stimuli revealed that two factors derived from these facial stimuli were correlated with two head orientations. The overall responses of the face neurons to direct gazes in the profile and frontal faces were significantly larger than that to averted gazes. The results suggest that information of both gaze and head direction is integrated in the amygdala, and that the amygdala is implicated in detection of direct gaze.     

威胁性情绪面孔对正常人脑的激活模式

目的:探讨正常人脑对威胁性情绪面孔的反应模式。方法:以愤怒和恐惧面孔为情绪刺激,在34名健康志愿受试者完成情绪面孔匹配任务的同时利用功能磁共振成像(fMRI)技术进行全脑数据采集。用SPM 8等软件处理功能成像数据,分析威胁性情绪面孔的脑区激活。结果:与威胁性情绪面孔视觉刺激加工相关的脑区主要分布在额叶皮质、颞叶、左侧杏仁核等,楔叶、枕叶等与视觉刺激相关脑区也有显著激活。结论:威胁性情绪面孔刺激对正常人脑的激活主要表现为左侧杏仁核、额叶、颞叶等多个脑区的协同加工机制。     

Structural encoding precludes recognition of face parts in prosopagnosia

The extent and the impact of spared processing of facial stimuli in the prosopagnosic patient LH is examined using the inversion effect and the face context effect. Our study asked how the deficit in individual face recognition is related to two perceptual abilities that are spared in this patient but between which there is interference when both are applied to the face stimulus, i.e. structural encoding of the face and parts-based matching procedures. Three experiments studied this relationship with task demands and stimulus properties designed to trigger the parts-based processes. In the first experiment, human and animal faces are presented upright or inverted with good performance only for the inverted condition. In Experiment 2 normals show a clear face context effect (matching of upright faces easier than scrambled or inverted ones) in the full face matching task whereas in the parts matching task the face superiority effect disappears. In contrast, LH shows a face inferiority effect when matching full faces but also when matching an isolated face part to a face part in a full face context. The results show that structural encoding of the face overrules parts-based procedures that could otherwise be helpful to tell individual faces apart.     

STRUCTURAL ENCODING PRECLUDES RECOGNITION OF FACE PARTS IN PROSOPAGNOSIA

The extent and the impact of spared processing of facial stimuli in the prosopagnosic patient LH is examined using the inversion effect and the face context effect. Our study asked how the deficit in individual face recognition is related to two perceptual abilities that are spared in this patient but between which there is interference when both are applied to the face stimulus, i.e. structural encoding of the face and parts-based matching procedures. Three experiments studied this relationship with task demands and stimulus properties designed to trigger the parts-based processes. In the first experiment, human and animal faces are presented upright or inverted with good performance only for the inverted condition. In Experiment 2 normals show a clear face context effect (matching of upright faces easier than scrambled or inverted ones) in the full face matching task whereas in the parts matching task the face superiority effect disappears. In contrast, LH shows a face inferiority effect when matching full faces but also when matching an isolated face part to a face part in a full face context. The results show that structural encoding of the face overrules parts-based procedures that could otherwise be helpful to tell individual faces apart.     

Gender-selective neural populations: evidence from event-related fMRI repetition suppression

Accurate recognition of gender in another individual is integral to successful human social interaction and to mate selection. When we encounter another person, we are effortlessly able to identify their gender, most often through the information conveyed by their facial features. Faces comprise the most abundantly encountered cue used to classify human gender. Considering the importance of facial information in gender perception, relatively little is known about the mechanisms involved in perceiving gender through human facial cues. We used an event-related fMRI repetition suppression paradigm to explore the neural circuitry underlying gender perception from facial information. Participants viewed brief consecutive images consisting of either gender-same face pairings (two male faces or two female faces) or images of gender-different face pairings (a male face preceded or followed by a female face), while attending to facial attractiveness in both conditions. Using a region-of-interest approach, we found repetition suppression on gender-same trials within the left ventral temporal fusiform gyrus and in the right collateral sulcus. Whole-brain voxel-wise analyses revealed selectivity for face gender again in the right collateral sulcus, in addition to the left cuneus and the right lateral occipital gyrus. Our results indicate that in addition to the face-selective FFA, cortical areas that are not traditionally considered to be “face-selective” are involved in the perception of gender-based facial cues.     

Brief Reports: Temporal stability of the error‐related negativity (ERN) and post‐error positivity (Pe): The role of number of trials

The error‐related negativity (ERN) and post‐error positivity (Pe) components of the event‐related potential (ERP) are relatively stable over time. The current study further assessed the temporal reliability of ERN and Pe amplitudes for random samples of 2 to 14 trials per participant and the grand mean over a 2‐week retest interval. In a replication of previous results, intraclass and zero‐order correlations revealed moderate to good temporal stability for participants' (N=20) grand mean ERN and Pe component amplitudes. Adding trials increased test–retest reliabilities; however, the temporal stability of ERN and Pe amplitudes with 14 or fewer trials were modest at best and considerably lower than that for the grand means. Overall, data support the temporal stability of grand‐mean ERN and Pe amplitudes and suggest that more than 14 trials are needed to include in ERN and Pe averages for adequate test–retest reliability.     

The Epworth sleepiness scale: Reliably unreliable in a sleep clinic population

The Epworth Sleepiness Scale is used frequently to measure excessive daytime sleepiness in research and clinical settings, although there is limited evidence on test–retest reliability, particularly among sleep clinic populations. The objective of this study was to evaluate the reliability of this instrument among adult patients recruited from a public hospital sleep clinic in Sydney, Australia. English‐speaking participants self‐completed the Epworth Sleepiness Scale on two occasions, at the specialist clinic visit and on the night of diagnostic polysomnography. Of the 108 participants included in the study, the majority were male (64%) and the mean age was 51 years. The median retest interval was 64 days. The primary outcome of test–retest reliability as measured using the intraclass correlation coefficient was 0.73 (95% confidence interval, 0.61–0.82). Despite moderate statistical reliability and a low mean difference of 1.1, Bland‐Altman analysis showed an unacceptably wide distribution of between‐score differences. The 95% limits of agreement were ?8.5 to +10.6, and an absolute difference in scores of at least 3 was observed in 60 (56%) of the participants. Our results suggest that the Epworth Sleepiness Scale should not be used in clinical settings to make individual‐level comparisons, such as the effect of therapeutic interventions, or to prioritise access to services.     

Own-sex effects in emotional memory for faces

The amygdala is known to be critical for the enhancement of memory for emotional, especially negative, material. Importantly, some researchers have suggested a sex-specific hemispheric lateralization in this process. In the case of facial expressions, another important factor that could influence memory success is the sex of the face, which could interact with the emotion depicted as well as with the sex of the perceiver. Whether this is the case remains unknown, as all previous studies of sex difference in emotional memory have employed affective pictures. Here we directly explored this question using functional magnetic resonance imaging in a subsequent memory paradigm for facial expressions (fearful, happy and neutral). Consistent with our hypothesis, we found that the hemispheric laterality of the amygdala involvement in successful memory for emotional material was influenced not only by the sex of the subjects, as previously proposed, but also by the sex of the faces being remembered. Namely, the left amygdala was more active for successfully remembered female fearful faces in women, whereas in men the right amygdala was more involved in memory for male fearful faces. These results confirm the existence of sex differences in amygdala lateralization in emotional memory but also demonstrate a subtle relationship between the observer and the stimulus in this process.     

Alexithymic features and automatic amygdala reactivity to facial emotion

Alexithymic individuals have difficulties in identifying and verbalizing their emotions. The amygdala is known to play a central role in processing emotion stimuli and in generating emotional experience. In the present study automatic amygdala reactivity to facial emotion was investigated as a function of alexithymia (as assessed by the 20-Item Toronto Alexithymia Scale). The Beck-Depression Inventory (BDI) and the State-Trait-Anxiety Inventory (STAI) were administered to measure participants' depressivity and trait anxiety. During 3T fMRI scanning, pictures of faces bearing sad, happy, and neutral expressions masked by neutral faces were presented to 21 healthy volunteers. The amygdala was selected as the region of interest (ROI) and voxel values of the ROI were extracted, summarized by mean and tested among the different conditions. A detection task was applied to assess participants' awareness of the masked emotional faces shown in the fMRI experiment. Masked sad and happy facial emotions led to greater right amygdala activation than masked neutral faces. The alexithymia feature difficulties identifying feelings was negatively correlated with the neural response of the right amygdala to masked sad faces, even when controlling for depressivity and anxiety. Reduced automatic amygdala responsivity may contribute to problems in identifying one's emotions in everyday life. Low spontaneous reactivity of the amygdala to sad faces could implicate less engagement in the encoding of negative emotional stimuli.     

Interhemispheric ERP asymmetries over inferior parietal cortex reveal differential visual working memory maintenance for fearful versus neutral facial identities

The goal of the present investigation was to discover whether visual working memory maintenance for faces is modulated by facial expression using event‐related potentials (ERPs). Each trial consisted of two sequential arrays, a memory array and a test array, each including either two or four faces with neutral or fearful expressions. The faces were displayed to the left and to the right of a central fixation cross. Two central arrows cued participants to encode one face or two faces displayed on one side of the memory array. The sustained posterior contralateral negativity (SPCN) component of the ERP time‐locked to the onset of the memory array was used as an index of visual working memory maintenance. Visual working memory performance was quantified using indexes of memory capacity (Cowan's K and K‐iterative), a standard index of sensitivity (d'), and reaction times (RTs). Relative to neutral faces, superior memory and longer change‐detection RTs to fearful face identities were observed when two faces were displayed on the cued side of the memory array. Fearful faces elicited an enhanced SPCN relative to neutral faces, especially when only one face was displayed on the cued side of the memory array. These findings suggest increased maintenance in visual working memory of faces with a fearful expression relative to faces with a neutral expression and that the representational format in which fearful faces are stored in memory may be characterized by enhanced resolution relative to that subtended in the maintenance of neutral faces.     

Increased amygdala activation is related to heart rate during emotion processing in adolescent subjects

Emotions have been conceptualized as representations of bodily responses to a stimulus that critically involves the autonomic nervous system (ANS). An association between amygdala activation and ANS activity has been shown in adults. However, to date, no studies have demonstrated this association in adolescents. Examining the interaction between the ANS and amygdala in healthy adolescents may provide information about age-related changes in the association between amygdala activation and ANS measures. Therefore, the aim of this study was to examine the relationship between amygdala activation and heart rate in normal adolescents. Eighteen 12- to 17-year old adolescents participated. Heart rate data was collected during functional magnetic resonance imaging while subjects performed a facial expression matching task that reliably activates the amygdala. Adolescents showed significant amygdala activation for all facial expressions relative to the shape-matching, control task. Moreover, the degree of activation in the right amygdala for Fearful faces was significantly correlated with heart rate (Spearman's rho=0.55, p=0.018, two-tailed). This study shows that amygdala activity is related to heart rate in healthy adolescents. Thus, similar to adults, adolescents show a coupling between processing emotional events and adjusting the ANS accordingly. Furthermore, this study confirms previous adolescent studies showing amygdala activation to Fearful, Angry, and Happy faces. Finally, the results of the present study lay the foundation for future research to investigate whether adolescents with mood or anxiety disorders show an altered coupling between processing emotionally salient events and ANS activity.     

Validity and reliability of a structured‐light 3D scanner and an ultrasound imaging system for measurements of facial skin thickness

Three‐dimensional (3 D)‐scanning‐based morphological studies of the face are commonly included in various clinical procedures. This study evaluated validity and reliability of a 3 D scanning system by comparing the ultrasound (US) imaging system versus the direct measurement of facial skin. The facial skin thickness at 19 landmarks was measured using the three different methods in 10 embalmed adult Korean cadavers. Skin thickness was first measured using the ultrasound device, then 3 D scanning of the facial skin surface was performed. After the skin on the left half of face was gently dissected, deviating slightly right of the midline, to separate it from the subcutaneous layer, and the harvested facial skin's thickness was measured directly using neck calipers. The dissected specimen was then scanned again, then the scanned images of undissected and dissected faces were superimposed using Morpheus Plastic Solution (version 3.0) software. Finally, the facial skin thickness was calculated from the superimposed images. The ICC value for the correlations between the 3 D scanning system and direct measurement showed excellent reliability (0.849, 95% confidence interval = 0.799–0.887). Bland‐Altman analysis showed a good level of agreement between the 3 D scanning system and direct measurement (bias = 0.49 ± 0.49 mm, mean±SD). These results demonstrate that the 3 D scanning system precisely reflects structural changes before and after skin dissection. Therefore, an in‐depth morphological study using this 3 D scanning system could provide depth data about the main anatomical structures of face, thereby providing crucial anatomical knowledge for utilization in various clinical applications. Clin. Anat. 30:878–886, 2017. © 2017 Wiley Periodicals, Inc.     

Social interest and the development of cortical face specialization: what autism teaches us about face processing

Investigations of face processing in persons with an autism spectrum disorder (ASD) inform upon theories of the development of "normal" face processing, and the story that emerges challenges some models of the nature and origin of cortical face specialization. Individuals with an ASD possess deficits in face processing and a lack of a fusiform face area (FFA). Evidence from studies of ASD can be conceptualized best using an expertise framework of face processing rather than models that postulate a face module in the fusiform gyrus. Because persons with an ASD have reduced social interest, they may fail to develop cortical face specialization. Face specialization may develop in normal individuals because they are socially motivated to regard the face, and such motivation promotes expertise for faces. The amygdala is likely the key node in the system that marks objects as emotionally salient and could be crucial to the development of cortical face specialization.     

Reliability and validity of the youth outcome questionnaire self‐report

The psychometric properties of an adolescent mental health outcome instrument (Youth Outcome Questionnaire Self‐Report version [Y‐OQ‐SR]) were examined. Participants were 206 adolescents (ages 12–18; mean age=15). The Y‐OQ‐SR was evaluated in terms of its internal consistency, test‐retest reliability, and concurrent validity. Criterion measures included the Behavior Assessment System for Children, Self‐Report of Personality—Adolescent Version (SRP), and the Child Behavior Checklist Youth Self Report (YSR). Analyses revealed very good internal consistency and test‐retest reliability of the Y‐OQ‐SR total score and subscales, and moderate to good concurrent validity with the SRP and YSR. The Y‐OQ‐SR appears to be a valid and reliable self‐report measure of psychosocial distress that warrants further study in youth psychotherapy research. © 2009 Wiley Periodicals, Inc. J Clin Psychol 65:1–12, 2009.     

The fusiform face area subserves face perception, not generic within-category identification

The function of the fusiform face area (FFA), a face-selective region in human extrastriate cortex, is a matter of active debate. Here we measured the correlation between FFA activity measured by functional magnetic resonance imaging (fMRI) and behavioral outcomes in perceptual tasks to determine the role of the FFA in the detection and within-category identification of faces and objects. Our data show that FFA activation is correlated on a trial-by-trial basis with both detecting the presence of faces and identifying specific faces. However, for most non-face objects (including cars seen by car experts), within-category identification performance was correlated with activation in other regions of the ventral occipitotemporal cortex, not the FFA. These results indicate that the FFA is involved in both detection and identification of faces, but that it has little involvement in within-category identification of non-face objects (including objects of expertise).