Deficits in facial, body movement and vocal emotional processing in autism spectrum disorders.

BACKGROUND: Previous behavioural and neuroimaging studies of emotion processing in autistic spectrum disorder (ASD) have focused on the use of facial stimuli. To date, however, no studies have examined emotion processing in autism across a broad range of social signals. METHOD: This study addressed this issue by investigating emotion processing in a group of 23 adults with ASD and 23 age- and gender-matched controls. Recognition of basic emotions ('happiness', 'sadness', 'anger', disgust' and 'fear') was assessed from facial, body movement and vocal stimuli. The ability to make social judgements (such as approachability) from facial stimuli was also investigated. RESULTS: Significant deficits in emotion recognition were found in the ASD group relative to the control group across all stimulus domains (faces, body movements and voices). These deficits were seen across a range of emotions. The ASD group were also impaired in making social judgements compared to the control group and this correlated with impairments in basic emotion recognition. CONCLUSIONS: This study demonstrates that there are significant and broad-ranging deficits in emotion processing in ASD present across a range of stimulus domains and in the auditory and visual modality; they cannot therefore be accounted for simply in terms of impairments in face processing or in the visual modality alone. These results identify a core deficit affecting the processing of a wide range of emotional information in ASD, which contributes to the impairments in social function seen in people with this condition.

A common neural system mediating two different forms of social judgement.

BACKGROUND: A wide range of neuropsychiatric conditions, including schizophrenia and autistic spectrum disorder (ASD), are associated with impairments in social function. Previous studies have shown that individuals with schizophrenia and ASD have deficits in making a wide range of social judgements from faces, including decisions related to threat (such as judgements of approachability) and decisions not related to physical threat (such as judgements of intelligence). We have investigated healthy control participants to see whether there is a common neural system activated during such social decisions, on the basis that deficits in this system may contribute to the impairments seen in these disorders. METHOD: We investigated the neural basis of social decision making during judgements of approachability and intelligence from faces in 24 healthy participants using functional magnetic resonance imaging (fMRI). We used conjunction analysis to identify common brain regions activated during both tasks. RESULTS: Activation of the amygdala, medial prefrontal cortex, inferior prefrontal cortex and cerebellum was seen during performance of both social tasks, compared to simple gender judgements from the same stimuli. Task-specific activations were present in the dorsolateral prefrontal cortex in the intelligence task and in the inferior and middle temporal cortex in the approachability task. CONCLUSIONS: The present study identified a common network of brain regions activated during the performance of two different forms of social judgement from faces. Dysfunction of this network is likely to contribute to the broad-ranging deficits in social function seen in psychiatric disorders such as schizophrenia and ASD.

The cutest little baby face: a hormonal link to sensitivity to cuteness in infant faces.

We used computer image manipulation to develop a test of perception of subtle gradations in cuteness between infant faces. We found that young women (19-26 years old) were more sensitive to differences in infant cuteness than were men (19-26 and 53-60 years old). Women aged 45 to 51 years performed at the level of the young women, whereas cuteness sensitivity in women aged 53 to 60 years was not different from that of men (19-26 and 53-60 years old). Because average age at menopause is 51 years in Britain, these findings suggest the possible involvement of reproductive hormones in cuteness sensitivity. Therefore, we compared cuteness discrimination in pre- and postmenopausal women matched for age and in women taking and not taking oral contraceptives (progestogen and estrogen). Premenopausal women and young women taking oral contraceptives (which raise hormone levels artificially) were more sensitive to variations of cuteness than their respective comparison groups. We suggest that cuteness sensitivity is modulated by female reproductive hormones.

Disgust in pre-clinical Huntington's disease: a longitudinal study.

Emotion recognition from both face and voice and experience of emotions were investigated in a group of non-symptomatic people at risk of carrying the Huntington's disease gene who presented for genetic testing. Based on the results of the DNA test, a group of people carrying the Huntington's disease gene (HD+), and a group of non-carriers (HD-) were formed. Since we were especially interested in the time course of possible deficits in emotion recognition, all people at risk were reassessed 6 and 12 months after the initial assessment. Recognising facial expressions of disgust was significantly impaired on all three assessments in the HD+ group, while recognition of vocal emotions and the experience of emotions were largely unaffected, confirming that deficits in recognition of facial expressions of disgust are an early correlate of carrying the gene for Huntington's disease. The inclusion of a healthy control group (n = 37) further allowed an estimate of the genetic and environmental contribution to deficits in facial emotion recognition.

Facial expression recognition in people with medicated and unmedicated Parkinson's disease.

Recognition of facial expressions of emotion was investigated in people with medicated and unmedicated Parkinson's disease (PD) and matched controls (unmedicated PD, n=16; medicated PD, n=20; controls, n=40). Participants in the medicated group showed some visual impairment (impaired contrast sensitivity) and performed less well on perception of unfamiliar face identity, but did not show significant deficits in the perception of sex, gaze direction, or familiar identity from the face. For both Parkinson's disease groups, there was evidence of impaired recognition of facial expressions in comparison to controls. These deficits were more consistently noted in the unmedicated group, who were also found to perform worse than the medicated group at recognising disgust from prototypical facial expressions, and at recognising anger and disgust in computer-manipulated images. Although both Parkinson's disease groups showed impairments of facial expression recognition, the consistently worse recognition of disgust in the unmedicated group is consistent with the hypothesis from previous studies that brain regions modulated by dopaminergic neurons are involved in the recognition of disgust.

Dissociation of affective modulation of recollective and perceptual experience following amygdala damage.

It has been suggested that similar neural mechanisms may underlie the affective modulation of both recollective and perceptual experience. A case is reported of a patient who has bilateral amygdala damage and marked impairment in the perception of emotion, particularly fear. The patient DR and 10 healthy control subjects (matched for school leaving age, intelligence quotient, and non-emotional memory performance) were shown a series of slides accompanied by an emotionally arousing narrative. One week later DR and the controls were given a surprise memory test for this material. In addition, they completed a verbal memory test using emotionally arousing stimuli. Both DR and the healthy control subjects showed a normative pattern of enhanced memory for emotional material. On the basis of these results and the previously demonstrated impairment of perception of emotion in this patient, it is concluded that different neural mechanisms may underlie affective modulation of recollective and perceptual experience.

Neuropsychology of fear and loathing.

For over 60 years, ideas about emotion in neuroscience and psychology have been dominated by a debate on whether emotion can be encompassed within a single, unifying model. In neuroscience, this approach is epitomized by the limbic system theory and, in psychology, by dimensional models of emotion. Comparative research has gradually eroded the limbic model, and some scientists have proposed that certain individual emotions are represented separately in the brain. Evidence from humans consistent with this approach has recently been obtained by studies indicating that signals of fear and disgust are processed by distinct neural substrates. We review this research and its implications for theories of emotion.

A principal component analysis of facial expressions.

Pictures of facial expressions from the Ekman and Friesen set (Ekman, P., Friesen, W. V., (1976). Pictures of facial affect. Palo Alto, California: Consulting Psychologists Press) were submitted to a principal component analysis (PCA) of their pixel intensities. The output of the PCA was submitted to a series of linear discriminant analyses which revealed three principal findings: (1) a PCA-based system can support facial expression recognition, (2) continuous two-dimensional models of emotion (e.g. Russell, J. A. (1980). A circumplex model of affect. Journal of Personality and Social Psychology, 39, 1161-1178) are reflected in the statistical structure of the Ekman and Friesen facial expressions, and (3) components for coding facial expression information are largely different to components for facial identity information. The implications for models of face processing are discussed.

Time courses of left and right amygdalar responses to fearful facial expressions.

Despite the many studies highlighting the role of the amygdala in fear perception, few have examined differences between right and left amygdalar responses. Using functional magnetic resonance imaging (fMRI), we examined neural responses in three groups of healthy volunteers (n = 18) to alternating blocks of fearful and neutral faces. Initial observation of extracted time series of both amygdalae to these stimuli indicated more rapid decreases of right than left amygdalar responses to fearful faces, and increasing magnitudes of right amygdalar responses to neutral faces with time. We compared right and left responses statistically by modeling each time series with (1) a stationary fit model (assuming a constant magnitude of amygdalar response to consecutive blocks of fearful faces) and (2) an adaptive model (no assumptions). Areas of significant sustained nonstationarity (time series points with significantly greater adaptive than stationary model fits) were demonstrated for both amygdalae. There was more significant nonstationarity of right than left amygdalar responses to neutral, and left than right amygdalar responses to fearful faces. These findings indicate significant variability over time of both right and left amygdalar responses to fearful and neutral facial expressions and are the first demonstration of specific differences in time courses of right and left amygdalar responses to these stimuli.

Impaired recognition and experience of disgust following brain injury.

Huntington's disease can particularly affect people's recognition of disgust from facial expressions, and functional neuroimaging research has demonstrated that facial expressions of disgust consistently engage different brain areas (insula and putamen) than other facial expressions. However, it is not known whether these particular brain areas process only facial signals of disgust or disgust signals from multiple modalities. Here we describe evidence, from a patient with insula and putamen damage, for a neural system for recognizing social signals of disgust from multiple modalities.

Caricaturing facial expressions.

The physical differences between facial expressions (e.g. fear) and a reference norm (e.g. a neutral expression) were altered to produce photographic-quality caricatures. In Experiment 1, participants rated caricatures of fear, happiness and sadness for their intensity of these three emotions; a second group of participants rated how 'face-like' the caricatures appeared. With increasing levels of exaggeration the caricatures were rated as more emotionally intense, but less 'face-like'. Experiment 2 demonstrated a similar relationship between emotional intensity and level of caricature for six different facial expressions. Experiments 3 and 4 compared intensity ratings of facial expression caricatures prepared relative to a selection of reference norms - a neutral expression, an average expression, or a different facial expression (e.g. anger caricatured relative to fear). Each norm produced a linear relationship between caricature and rated intensity of emotion; this finding is inconsistent with two-dimensional models of the perceptual representation of facial expression. An exemplar-based multidimensional model is proposed as an alternative account.

Configural information in facial expression perception.

Composite facial expressions were prepared by aligning the top half of one expression (e.g., anger) with the bottom half of another (e.g., happiness). Experiment 1 shows that participants are slower to identify the expression in either half of these composite images relative to a "noncomposite" control condition in which the 2 halves are misaligned. This parallels the composite effect for facial identity (A. W. Young, D. Hellawell, & D. C. Hay, 1987), and like its identity counterpart, the effect is disrupted by inverting the stimuli (Experiment 2). Experiment 3 shows that no composite effect is found when the top and bottom sections contain different models' faces posing the same expression; this serves to exclude many nonconfigural interpretations of the composite effect (e.g., that composites are more "attention-grabbing" than noncomposites). Finally, Experiment 4 demonstrates that the composite effects for identity and expression operate independently of one another.

Facial expression recognition by people with mobius syndrome.

We present an investigation of facial expression recognition by three people (BC, LP, and NC) with Mobius syndrome, a congenital disorder producing facial paralysis. The participants were asked to identify the emotion displayed in 10 examples of facial expressions associated with each of 6 basic emotions from the Ekman and Friesen (1976) series. None of the three people with Mobius syndrome was significantly impaired on this task. On a second test of facial expression recognition using computer-morphed facial expressions, NC showed a statistically significant impairment, BC a borderline deficit, and LP was unimpaired. However, even when impairments were found, people with Mobius syndrome still recognised many of the facial expressions shown to them. The recognition of facial expressions by people who have never been able to produce such signals on their own faces demonstrates that the ability to produce facial expressions is not a necessary prerequisite of their recognition.

Recognition of facial emotion in nine individuals with bilateral amygdala damage.

Findings from several case studies have shown that bilateral amygdala damage impairs recognition of emotions in facial expressions, especially fear. However, one study did not find such an impairment, and, in general, comparison across studies has been made difficult because of the different stimuli and tasks employed. In a collaborative study to facilitate such comparisons, we report here the recognition of emotional facial expressions in nine subjects with bilateral amygdala damage, using a sensitive and quantitative assessment. Compared to controls, the subjects as a group were significantly impaired in recognizing fear, although individual performances ranged from severely impaired to essentially normal. Most subjects were impaired on several negative emotions in addition to fear, but no subject was impaired in recognizing happy expressions. An analysis of response consistency showed that impaired recognition of fear could not be attributed simply to mistaking fear for another emotion. While it remains unclear why some subjects with amygdala damage included here are not impaired on our task, the results overall are consistent with the idea that the amygdala plays an important role in triggering knowledge related to threat and danger signaled by facial expressions.

Dyspraxia in a patient with corticobasal degeneration: the role of visual and tactile inputs to action.

OBJECTIVES: To investigate the roles of visual and tactile information in a dyspraxic patient with corticobasal degeneration (CBD) who showed dramatic facilitation in miming the use of a tool or object when he was given a tool to manipulate; and to study the nature of the praxic and neuropsychological deficits in CBD. METHODS: The subject had clinically diagnosed CBD, and exhibited alien limb behaviour and striking ideomotor dyspraxia. General neuropsychological evaluation focused on constructional and visuospatial abilities, calculation, verbal fluency, episodic and semantic memory, plus spelling and writing because impairments in this domain were presenting complaints. Four experiments assessed the roles of visual and tactile information in the facilitation of motor performance by tools. Experiment 1 evaluated the patient's performance of six limb transitive actions under six conditions: (1) after he described the relevant tool from memory, (2) after he was shown a line drawing of the tool, (3) after he was shown a real exemplar of the tool, (4) after he watched the experimenter perform the action, (5) while he was holding the tool, and (6) immediately after he had performed the action with the tool but with the tool removed from his grasp. Experiment 2 evaluated the use of the same six tools when the patient had tactile but no visual information (while he was blindfolded). Experiments 3 and 4 assessed performance of actions appropriate to the same six tools when the patient had either neutral or inappropriate tactile feedback-that is, while he was holding a non-tool object or a different tool. RESULTS: Miming of tool use was not facilitated by visual input; moreover, lack of visual information in the blindfolded condition did not reduce performance. The principal positive finding was a dramatic facilitation of the patient's ability to demonstrate object use when he was holding either the appropriate tool or a neutral object. Tools inappropriate to the requested action produced involuntary performance of the stimulus relevant action. CONCLUSIONS: Tactile stimulation was paramount in the facilitation of motor performance in tool use by this patient with CBD. This outcome suggests that tactile information should be included in models which hypothesise modality specific inputs to the action production system. Significant impairments in spelling and letter production that have not previously been reported in CBD have also been documented.

Knowing no fear.

People with brain injuries involving the amygdala are often poor at recognizing facial expressions of fear, but the extent to which this impairment compromises other signals of the emotion of fear has not been clearly established. We investigated N.M., a person with bilateral amygdala damage and a left thalamic lesion, who was impaired at recognizing fear from facial expressions. N.M. showed an equivalent deficit affecting fear recognition from body postures and emotional sounds. His deficit of fear recognition was not linked to evidence of any problem in recognizing anger (a common feature in other reports), but for his everyday experience of emotion N.M. reported reduced anger and fear compared with neurologically normal controls. These findings show a specific deficit compromising the recognition of the emotion of fear from a wide range of social signals, and suggest a possible relationship of this type of impairment with alterations of emotional experience.

Neural responses to facial and vocal expressions of fear and disgust.

Neuropsychological studies report more impaired responses to facial expressions of fear than disgust in people with amygdala lesions, and vice versa in people with Huntington's disease. Experiments using functional magnetic resonance imaging (fMRI) have confirmed the role of the amygdala in the response to fearful faces and have implicated the anterior insula in the response to facial expressions of disgust. We used fMRI to extend these studies to the perception of fear and disgust from both facial and vocal expressions. Consistent with neuropsychological findings, both types of fearful stimuli activated the amygdala. Facial expressions of disgust activated the anterior insula and the caudate-putamen; vocal expressions of disgust did not significantly activate either of these regions. All four types of stimuli activated the superior temporal gyrus. Our findings therefore (i) support the differential localization of the neural substrates of fear and disgust; (ii) confirm the involvement of the amygdala in the emotion of fear, whether evoked by facial or vocal expressions; (iii) confirm the involvement of the anterior insula and the striatum in reactions to facial expressions of disgust; and (iv) suggest a possible general role for the perception of emotional expressions for the superior temporal gyrus.

Face processing impairments after encephalitis: amygdala damage and recognition of fear.

Face processing and facial emotion recognition were investigated in five post-encephalitic people of average or above-average intelligence. Four of these people (JC, YW, RB and SE) had extensive damage in the region of the amygdala. A fifth post-encephalitic person with predominantly hippocampal damage and relative sparing of the amygdala (RS) participated, allowing us to contrast the effects of temporal lobe damage including and excluding the amygdala region. The findings showed impaired recognition of fear following bilateral temporal lobe damage when this included the amygdala. For JC, this was part of a constellation of deficits on face processing tasks, with impaired recognition of several emotions. SE, YW and RB, however, showed relatively circumscribed deficits. Although they all had some problems in recognizing or naming famous faces, and had poor memory for faces on the Warrington Recognition Memory Test, none showed a significant impairment on the Benton Test of Facial Recognition, indicating relatively good perception of the face's physical structure. In a test of recognition of basic emotions (happiness, surprise, fear, sadness, disgust and anger), SE, YW and RB achieved normal levels of performance in comparison to our control group for all emotions except fear. Their results contrast with those of RS, with relative sparing of the amygdala region and unimpaired recognition of emotion, pointing clearly toward the importance of the amygdala in the recognition of fear.

A neuromodulatory role for the human amygdala in processing emotional facial expressions.

Localized amygdalar lesions in humans produce deficits in the recognition of fearful facial expressions. We used functional neuroimaging to test two hypotheses: (i) that the amygdala and some of its functionally connected structures mediate specific neural responses to fearful expressions; (ii) that the early visual processing of emotional faces can be influenced by amygdalar activity. Normal subjects were scanned using PET while they performed a gender discrimination task involving static grey-scale images of faces expressing varying degrees of fear or happiness. In support of the first hypothesis, enhanced activity in the left amygdala, left pulvinar, left anterior insula and bilateral anterior cingulate gyri was observed during the processing of fearful faces. Evidence consistent with the second hypothesis was obtained by a demonstration that amygdalar responses predict expression-specific neural activity in extrastriate cortex.

The effect of self-referent material on the reasoning of people with delusions.

People with delusions have been shown to have both generalized (Huq, Garety & Hemsley, 1988) and content-specific biases in reasoning (Bentall, 1994). Our concern here was whether the hastiness that has been found when people with delusions reason on relatively abstract tasks would be present on a more realistic task. A second concern was whether reasoning with salient or emotional material would increase the hastiness bias in people with delusions. Two versions of a probabilistic reasoning task were used to study the data gathering of people with delusions. The first version employed realistic but emotionally neutral material. People with delusions requested less evidence before making a decision than psychiatric and normal comparison groups. Therefore, the hastiness found previously with abstract materials was seen to generalize to a more realistic task. In the second version participants were required to reason with material that had an emotional content and may have been regarded as being personally meaningful. In this condition all groups reduced the amount of evidence requested before making a decision.