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Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies.

This article reviews behavioral and electrophysiological studies of face processing and discusses hypotheses for understanding the nature of face processing impairments in autism. Based on results of behavioral studies, this study demonstrates that individuals with autism have impaired face discrimination and recognition and use atypical strategies for processing faces characterized by reduced attention to the eyes and piecemeal rather than configural strategies. Based on results of electrophysiological studies, this article concludes that face processing impairments are present early in autism, by 3 years of age. Such studies have detected abnormalities in both early (N170 reflecting structural encoding) and late (NC reflecting recognition memory) stages of face processing. Event-related potential studies of young children and adults with autism have found slower speed of processing of faces, a failure to show the expected speed advantage of processing faces versus nonface stimuli, and atypical scalp topography suggesting abnormal cortical specialization for face processing. Other electrophysiological studies have suggested that autism is associated with early and late stage processing impairments of facial expressions of emotion (fear) and decreased perceptual binding as reflected in reduced gamma during face processing. This article describes two types of hypotheses-cognitive/perceptual and motivational/affective--that offer frameworks for understanding the nature of face processing impairments in autism. This article discusses implications for intervention.

Autistic Disorder↗

Differential attentional guidance by unattended faces expressing positive and negative emotion.

Four experiments were conducted to evaluate whether focal attention can be guided by an analysis of the emotional expression in a face. Participants searched displays of 7, 11, 15, and 19 schematic faces for the location of a unique face expressing either a positive or a negative emotion located among distractor faces expressing a neutral emotion. The slopes of the search functions for locating the negative face were shallower than the slopes of the search functions for locating the positive face (Experiments 1A and 2A). When the faces were inverted to reduce holistic face perception, the slopes of the search functions for locating positive and negative faces were not different (Experiments 1B and 2B). The results suggest that the emotional expression in a face can be perceived outside the focus of attention and can guide focal attention to the location of the face.

Adult↗

Recognition of faces expressing emotions in patients with unilateral brain damage.

The experiment concerned the functional specialization of brain hemispheres in recognizing faces expressing emotions in patients with focal brain damage of the left and right hemispheres and in persons without damage of the central nervous system. Three types of faces were presented: happy i.e. expressing positive emotions, sad i.e. expressing negative emotions and neutral. The task of the subject was to recognize the test face exposed for 20 ms in the left or right visual field and point to the correct face on the response-card which contained three different faces. The errors made in recognizing of faces exposed in the right visual field (addressing the left hemisphere) and in the left one (addressing the right hemisphere) were analyzed. The patients with left hemisphere damage showed a similar pattern of hemispheric differences to that observed in the controls. In case of neutral and sad faces fewer errors were made in the left visual field exposures, in case of happy faces no significant differences between the two fields were stated. The results in patients with right hemispheric damage were different from both the other groups. In processing all the three types of faces, fewer errors were made in the left visual field presentations independently of the localization of the damage within the right hemisphere. Similar recognition level of different types of faces was also found in patients with left or right hemisphere damage as well as in controls. The above results suggest the crucial role of the right hemisphere in processing both positive and negative emotions expressed in faces.

Adult↗

[The effects on upper first molars by the face-bow construction. Consideration of utilizing the strain gauge method and the computer method of structural analysis].

The present study was undertaken for the purpose of detecting the influence on upper first molars by the dynamic behavior originated in face-bow construction. Tests were made at occipital pull and cervical pull face-bows utilizing strain gauge method and the computer method of structural analysis. As for the occipital pull face-bow, a short outer-bow 35 mm frontward of a tube was bent 30 degrees upward and be pulled in that direction. As for the cervical pull face-bow, a medium outer-bow flash to tube, parallel to the inner-bow was pulled from 20 degrees downward. These two types of face-bows were divided into 4 types, those with loops at the back end (WL) and to those without loops (NL). In the strain gauge method, the force and moment to tubes was measured and compared with the values obtained from theoretical analysis. And in the structural analysis, the data of deflection was compared with each other. Those results indicated that 1. face-bow shows a different force to the molars and a different phase of deflection, according to the difference of it's force concentrative section. 2. the larger the deflection, the larger the deviation of forces on molars from theoretical values. 3. the way of setting loops against the direction of pull alters the phase of deflection of face-bow and the force on molars. 4. existance of loops at inner-bow affects as follows: (1) Reduction of moment of each type of face-bow. (2) Reduction of vertical force at occipital pull face-bow and it's increase at cervical pull face-bow. (3) Resistance for deflection of face-bows in the case of tractive force for closing loops.

Dental Stress Analysis↗

Visual neurones responsive to faces in the monkey temporal cortex.

Of 497 single neurones recorded in the cortex in the fundus of the superior temporal sulcus (STS) of three alert rhesus monkeys, a population of at least 48 cells which were selectively responsive to faces had the following response properties: (1) The cells' responses to faces (real or projected, human or rhesus monkey) were two to ten times as large as those to gratings, simple geometrical stimuli or complex 3-D objects. (2) Neuronal responses to faces were excitatory, sustained and were time-locked to the stimulus presentation with a latency of between 80 and 160 ms. (3) The cells were unresponsive to auditory or tactile stimuli and to the sight of arousing or aversive stimuli. (4) The magnitude of the responses of 28 cells tested was relatively constant despite transformations, such as rotation, so that the face was inverted or horizontal, and alterations of colour, size or distance. (5) Rotation to profile substantially reduced the responses of 21 cells (31 tested). (6) Masking out or presenting parts of the face (i.e. eyes, mouth or hair) in isolation revealed that different cells responded to different features or subsets of features. (7) For several cells, responses to the normal organisation of cut-out or line-drawn facial features were significantly larger than to jumbled controls. These findings indicate that explanations in terms of arousal, emotional or motor reactions, simple visual feature sensitivity or receptive fields are insufficient to account for the selective responses to faces and face features observed in this population of STS neurones. It appears that these neurones are part of a system specialised to code for faces or features present in faces, and it is suggested that damage to this system is related to prosopagnosia, or difficulty in face recognition, in man and to the tameness and social disturbances which follow temporal lobe damage and are part of the Klüver-Bucy syndrome in the monkey.

Animals↗

Accelerated recognition of left oblique views of faces.

Because faces in portraits are depicted more frequently in a left rather than a right oblique (half-profile or 3/4) view, we addressed the question of whether people find it easier to recognize the left or right 3/4 view of a familiar person's face. We examined the ability of 13 subjects to match familiar faces that were presented in either the left or right 3/4 view, with names that were presented either before or after the faces (face-name and name-face matching tasks, respectively). In both tasks, the subjects responded more rapidly to a left than to a right 3/4 view of the same face. This suggests that during face recognition the processing of information from faces that are presented in the left 3/4 view is dominant over the processing of right 3/4 views of familiar faces.

Adult↗

Face-selective and auditory neurons in the primate orbitofrontal cortex.

Neurons with responses selective for faces are described in the macaque orbitofrontal cortex. The neurons typically respond 2-13 times more to the best face than to the best non-face stimulus, and have response latencies which are typically in the range of 130-220 ms. Some of these face-selective neurons respond to identity, and others to facial expression. Some of the neurons do not have different responses to different views of a face, which is a useful property of neurons responding to face identity. Other neurons have view-dependent responses, and some respond to moving but not still heads. The neurons with face expression, face movement, or face view-dependent responses would all be useful as part of a system decoding and representing signals important in social interactions. The representation of face identity is also important in social interactions, for it provides some of the information needed in order to make different responses to different individuals. In addition, some orbitofrontal cortex neurons were shown to be tuned to auditory stimuli, including for some neurons, the sound of vocalizations. The findings are relevant to understanding the functions of the primate including human orbitofrontal cortex in normal behaviour, and to understanding the effects of damage to this region in humans.

Acoustic Stimulation↗

Longer fixation duration while viewing face images.

The spatio-temporal properties of saccadic eye movements can be influenced by the cognitive demand and the characteristics of the observed scene. Probably due to its crucial role in social communication, it is argued that face perception may involve different cognitive processes compared with non-face object or scene perception. In this study, we investigated whether and how face and natural scene images can influence the patterns of visuomotor activity. We recorded monkeys' saccadic eye movements as they freely viewed monkey face and natural scene images. The face and natural scene images attracted similar number of fixations, but viewing of faces was accompanied by longer fixations compared with natural scenes. These longer fixations were dependent on the context of facial features. The duration of fixations directed at facial contours decreased when the face images were scrambled, and increased at the later stage of normal face viewing. The results suggest that face and natural scene images can generate different patterns of visuomotor activity. The extra fixation duration on faces may be correlated with the detailed analysis of facial features.

Analysis of Variance↗

Cardiovascular responses to cold-water immersions of the forearm and face, and their relationship to apnoea.

Apnoea as well as cold stimulation of the face or the extremities elicits marked cardiovascular reflexes in humans. The purpose of this study was to investigate whether forearm immersion in cold water has any effect on the cardiovascular responses to face immersion and apnoea. We recorded cardiovascular responses to coldwater immersions of the forearm and face in 19 (part I) and 23 subjects (part II). The experimental protocol was divided in two parts, each part containing four tests: I1, forearm immersion during eupnoea; I2, face immersion during eupnoea; I3, forearm and face immersion during eupnoea; I4, face immersion during apnoea; II1, apnoea without immersion; II2, forearm immersion during apnoea; II3, face immersion during apnoea; and II4, forearm and face immersion during apnoea. The water temperature was 9-11 degrees C. Cold-water immersion of either the forearm or face was enough to elicit the most pronounced thermoregulatory vasoconstriction during both eupnoea and apnoea. During eupnoea, heart rate responses to forearm immersion (3% increase) and face immersion (9% decrease) were additive during concurrent stimulation (3% decrease). During apnoea, the heart rate responses were not affected by the forearm immersion. The oxygen-conserving diving response seems to dominate over thermoregulatory responses in the threat of asphyxia. During breathing, however, the diving response serves no purpose and does not set thermoregulatory adjustments aside.

Adult↗

Recognition of unfamiliar faces in prosopagnosia.

Prosopagnosia is clinically defined as a specific and extreme inability to recognize familiar faces. However, doubts have been expressed concerning prosopagnosics' preserved ability to recognize unfamiliar faces and to make other within category discriminations. The present study pursues these doubts. If recognition of unfamiliar faces and objects is intact, then prosopagnosics should demonstrate normal processing for all tasks that depend on the possession of intact stored visual descriptions at the category level. In particular, they should show normal face and object superiority effects. A detailed investigation was carried out on a well documented prosopagnosic (KD) and less extensively on three other (RB, AH and OA) well attested cases. Experiments 1 and 2 considered whether face and object superiority effects were observed in these patients. No difference in the pattern of recognition performance was found between normal and unusual arrangements of faces and objects. Their pattern of performance differed both from unilateral brain-damaged patients and normal controls. The results suggest both that these prosopagnosic patients were impaired on the recognition of unfamiliar faces and that their problem is not specific to faces. Experiment 3 showed that KD was impaired on a face/non-face decision task but appeared to benefit by the stimulus being presented in the normal orientation. For normal controls, mental rotation of a face appeared to be a separate process from face categorization. Experiment 4 found that KD, AH and OA were impaired, compared to normal controls, in their ability to recognize emotional expressions but not more than brain-damaged controls. The impairment of the prosopagnosics tested in the present study is placed at the interaction between stored object descriptions and the structural encoding stage of Bruce and Young. Consideration is given to an elaboration of the structural encoding stage in which boundary (category defining) information is separately processed from surface (detailed texture) information.

Agnosia↗

Gaze motor asymmetries in the perception of faces during a memory task.

In 33 male and female adult volunteers, eye position recordings were performed by means of an infrared reflection technique. Slides of randomly shuffled black-and-white photographs (7.5 x 10 degrees) of faces and vases were projected for 6 or 20 sec respectively in a visual memory task. In each series, 10 slides of art nouveau vases and of the "inner part" of masked Caucasian faces were used. During recording the head was fixed by a bite-board. (a) For faces the preferred targets of the centre of gaze were the eyes, the mouth and nose region, for vases the contours and some prominent ornaments. (b) Left-right asymmetries in the gaze-movement sampling strategy appeared with faces, but not with vases. In faces, the overall time that the centre of gaze remained in the left half of the field of gaze was significantly longer than in the right half. (c) When, however, the amplitude of the gaze excursions into the left and right halves of the inspected items was taken as a measure and normalized, a preference for the right gaze field was observed. (d) The relative left-right bias during face inspection was stronger with the 6 sec than with the 20 sec inspection period and significantly stronger in female than in male subjects for the 6 sec tasks. (e) Left/right inversion of the face stimuli did not abolish the side bias. Thus the asymmetric sampling strategy when faces were inspected as compared to vases was due to "internal" factors on the part of the subjects. It is hypothesized that a left-right asymmetry in hemispheric visual data processing for face stimuli was the cause of a left-right asymmetry in gaze motor strategies when faces were inspected.

Adult↗

Neurons in the amygdala of the monkey with responses selective for faces.

To investigate the functions of the amygdala in visual information processing and in emotional and social responses, recordings were made from single neurons in the amygdala of the monkey. A population of neurons (40 of more than 1000 recorded in 4 monkeys) was investigated which responded primarily to faces. These neurons typically (1) responded to some human or monkey faces, which were presented to the monkey through a large aperture shutter so that response latencies could be measured, or were simply shown to the monkey, (2) responded to 2-dimensional representations of these faces, as well as to real 3-dimensional faces, (3) had no responses or only small (less than half maximum) responses to gratings, simple geometrical, other complex 3-D stimuli, or to arousing and aversive stimuli, (4) had response latencies of 110-200 ms, (5) were located in the basal accessory nucleus of the amygdala, (6) responded differently to different faces, as shown by measures of d', and could thus over a population of such neurons code information useful for making different responses to different individuals, (7) could in some cases (9/11 tested) respond to parts of faces, and (8) in a few cases (4/19 tested) responded more to a face which produced an emotional response. A comparison made in three monkeys of the responses of these neurons with the responses of 77 neurons with face-selective responses recorded in the cortex of the superior temporal sulcus (STS) showed that the amygdaloid neurons had longer response latencies (110-200 compared to 90-140 ms), and were in some respects more selective in their responses to different faces. It is suggested that the deficits in social and emotional behavior produced by amygdala lesions could be due in part to damage to a neuronal system specialized in utilizing information from faces so that appropriate social and emotional responses can be made to different individuals.

Amygdala↗

Perceptual asymmetries in left- and right-handers for cartoon and real faces.

We examined 40 left-handers and 40 right-handers on two free-vision tests of face processing. A chimeric face composed of a smiling half-face joined to either a neutral half-face (real faces) or a sad half-face (cartoon faces) and its mirror image were presented on each trial. Subjects judged which chimeric face looked happier, the one with the smile to the left or the one with the smile to the right. Right-handers, but not left-handers, had a highly significant leftward attentional bias, since chimeras with the smile to the left were judged happier than those with the smile to the right. The cartoon- and real-face tasks did not differ in the mean perceptual asymmetries they elicited. However, correlations between attentional-asymmetry scores for the two tasks, although high for both left- and right-handers, were significantly smaller than task reliabilities. Thus, the cartoon- and real-face tasks overlap to a major extent in the lateralized processes they measure, but to a lesser extent, they also index different lateralized processes.

Adult↗

Attentional capture by task-irrelevant fearful faces is revealed by the N2pc component.

We measured the N2pc component as an electrophysiological indicator of attentional selection to investigate whether fearful faces can attract attention even when they are entirely task-irrelevant and attention is focused on another demanding visual monitoring task. Participants had to detect infrequent luminance changes of the fixation cross, while ignoring stimulus arrays containing a face singleton (a fearful face among neutral faces, or neutral face among fearful faces) to the left or right of fixation. On trials without a target luminance change, an N2pc was elicited by fearful faces presented next to fixation, irrespective of whether they were singletons or not, demonstrating that irrelevant fearful faces can bias the spatial distribution of attention. The N2pc to fearful faces was attenuated when face arrays were presented simultaneously with a target luminance change, suggesting that concurrent target processing reduces attentional capture by emotional salient events.

Adult↗

"Did you see him in the newspaper?" Electrophysiological correlates of context and valence in face processing.

Face recognition emerges from an interaction between bottom-up and top-down processing. Specifically, it relies on complex associations between the visual representation of a given face and previously stored knowledge about that face (e.g. biographical details). In the present experiment, the time-course of the interaction between bottom-up and top-down processing was investigated using event-related potentials (ERPs) and manipulating realistic, ecological contextual information. In the study phase, half of the faces (context faces) were framed in a newspaper page entitled with an action committed by the person depicted; these actions could have a positive or a negative value, so in this way emotional valence could be manipulated. The other half was presented on a neutral background (no-context faces). In the test phase, previously presented faces and new ones were presented on neutral backgrounds and an old/new discrimination was requested. The N170 component was modulated by both context (presence/absence at encoding) and valence (positive/negative). A reduction in amplitude was found for context faces as opposed to no-context faces. The same pattern was observed for negative faces compared to positive ones. Moreover, later activations associated with context and valence were differentially distributed over the scalp: context effects were prominent in left frontal areas, traditionally linked to person-specific information retrieval, whereas valence effects were broadly distributed over the scalp. In relation to recent neuroimaging findings on the neural basis of top-down modulations, present findings indicate that the information flow from higher-order areas might have modulated the N170 component and mediated the retrieval of semantic information pertaining to the study episode.

Brain Mapping↗

Face perception is modulated by sexual preference.

Face perception is mediated by a distributed neural system in the human brain . The response to faces is modulated by cognitive factors such as attention, visual imagery, and emotion ; however, the effects of gender and sexual orientation are currently unknown. We used fMRI to test whether subjects would respond more to their sexually preferred faces and predicted such modulation in the reward circuitry. Forty heterosexual and homosexual men and women viewed photographs of male and female faces and assessed facial attractiveness. Regardless of their gender and sexual orientation, all subjects similarly rated the attractiveness of both male and female faces. Within multiple, bilateral face-selective regions in the visual cortex, limbic system, and prefrontal cortex, similar patterns of activation were found in all subjects in response to both male and female faces. Consistent with our hypothesis, we found a significant interaction between stimulus gender and the sexual preference of the subject in the thalamus and medial orbitofrontal cortex, where heterosexual men and homosexual women responded more to female faces and heterosexual women and homosexual men responded more to male faces. Our findings suggest that sexual preference modulates face-evoked activation in the reward circuitry.

Brain↗

Pressure on the face while in the prone position: ProneView versus Prone Positioner.

STUDY OBJECTIVE: To measure the surface pressure on the face of a patient placed in the prone position with the most commonly used prone positioning devices, a non-face-contoured positioner (PP) and a new face-contoured device (PV). DESIGN: Prospective, randomized comparison. SETTING: Operating room in an American academic medical center. SUBJECTS: 35 randomly recruited adult volunteers. INTERVENTIONS: Surface pressure on the face was measured in awake subjects placed in the prone position, with the head and neck in the position of most comfort, using both the PP and PV devices. MEASUREMENTS: Surface pressure was obtained using an array of small transducers imbedded in a thin cushion that was interfaced between the face and positioning device. The amount of extension or flexion of the head on the neck was estimated using an angular measurement of eye-ear line and horizontal line. MAIN RESULTS: The average surface pressure on the face was less with the PV than with the PP (21 +/- 3 mmHg vs. 27 +/- 5 mmHg; p < 0.0001). The number of areas where pressure exceeded 30 mmHg and 50 mmHg was lower for the PV than the PP (15 +/- 7.5 areas vs. 19 +/- 7.2 areas > 30 mmHg; p < 0.05; 5.2 +/- 3.3 areas vs. 9.0 +/- 5.0 areas > 50 mmHg; p < 0.0001). Pressure on the chin increased with extension of the head or neck (p < 0.05) with both devices. CONCLUSIONS: Surface pressure on the face in the prone position is 29% higher with the non-face-contoured PP than with the face-contoured PV. The number of areas on the face where the surface pressure is greater than 50 mmHg is 80% higher with the PP than the PV. Small degrees of head extension increases pressure on the chin. Both devices produce areas of pressure, typically over the chin, which may be associated with local skin damage. Keeping the head and neck in a non-flexed, non-extended position may minimize pressures.

Equipment Design↗

Neural responses to Mooney images reveal a modular representation of faces in human visual cortex.

The way in which information about objects is represented in visual cortex remains controversial. One model of human object recognition poses that information is processed in modules, highly specialised for different categories of objects; an opposing model appeals to a distributed representation across a large network of visual areas. We addressed this debate by monitoring activity in face- and object-selective areas while human subjects viewed ambiguous face stimuli (Mooney faces). The measured neural response in the face-selective region of the fusiform gyrus was greater when subjects reported seeing a face than when they perceived the image as a collection of blobs. In contrast, there was no difference in magnetic resonance response between face and no-face perceived events in either the face-selective voxels of the superior temporal sulcus or the object-selective voxels of the parahippocampal gyrus and lateral occipital complex. These results challenge the concept that neural representation of faces is distributed and overlapping and suggest that the fusiform gyrus is tightly linked to the awareness of faces.

Adult↗