Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge.

Functional magnetic resonance imaging (fMRI) of the human brain was used to study whether the amygdala is activated in response to emotional stimuli, even in the absence of explicit knowledge that such stimuli were presented. Pictures of human faces bearing fearful or happy expressions were presented to 10 normal, healthy subjects by using a backward masking procedure that resulted in 8 of 10 subjects reporting that they had not seen these facial expressions. The backward masking procedure consisted of 33 msec presentations of fearful or happy facial expressions, their offset coincident with the onset of 167 msec presentations of neutral facial expressions. Although subjects reported seeing only neutral faces, blood oxygen level-dependent (BOLD) fMRI signal in the amygdala was significantly higher during viewing of masked fearful faces than during the viewing of masked happy faces. This difference was composed of significant signal increases in the amygdala to masked fearful faces as well as significant signal decreases to masked happy faces, consistent with the notion that the level of amygdala activation is affected differentially by the emotional valence of external stimuli. In addition, these facial expressions activated the sublenticular substantia innominata (SI), where signal increases were observed to both fearful and happy faces--suggesting a spatial dissociation of territories that respond to emotional valence versus salience or arousal value. This study, using fMRI in conjunction with masked stimulus presentations, represents an initial step toward determining the role of the amygdala in nonconscious processing.

Facial expression megamix: tests of dimensional and category accounts of emotion recognition.

We report four experiments investigating the perception of photographic quality continua of interpolated ('morphed') facial expressions derived from prototypes of the 6 emotions in the Ekman and Friesen (1976) series (happiness, surprise, fear, sadness, disgust and anger). In Experiment 1, morphed images made from all possible pairwise combinations of expressions were presented in random order; subjects identified these as belonging to distinct expression categories corresponding to the prototypes at each end of the relevant continuum. This result was replicated in Experiment 2, which also included morphs made from a prototype with a neutral expression, and allowed 'neutral' as a response category. These findings are inconsistent with the view that facial expressions are recognised by locating them along two underlying dimensions, since such a view predicts that at least some transitions between categories should involve neutral regions or identification as a different emotion. Instead, they suggest that facial expressions of basic emotions are recognised by their fit to discrete categories. Experiment 3 used continua involving 6 emotions to demonstrate best discrimination of pairs of stimuli falling across category boundaries; this provides further evidence of categorical perception of facial expressions of emotion. However, in both Experiment 1 and Experiment 2, reaction time data showed that increasing distance from the prototype had a definite cost on ability to identify emotion in the resulting morphed face. Moreover, Experiment 4 showed that subjects had some insight into which emotions were blended to create specific morphed images. Hence, categorical perception effects were found even though subjects were sensitive to physical properties of these morphed facial expressions. We suggest that rapid classification of prototypes and better across boundary discriminability reflect the underlying organisation of human categorisation abilities.

Response and habituation of the human amygdala during visual processing of facial expression.

We measured amygdala activity in human volunteers during rapid visual presentations of fearful, happy, and neutral faces using functional magnetic resonance imaging (fMRI). The first experiment involved a fixed order of conditions both within and across runs, while the second one used a fully counterbalanced order in addition to a low level baseline of simple visual stimuli. In both experiments, the amygdala was preferentially activated in response to fearful versus neutral faces. In the counterbalanced experiment, the amygdala also responded preferentially to happy versus neutral faces, suggesting a possible generalized response to emotionally valenced stimuli. Rapid habituation effects were prominent in both experiments. Thus, the human amygdala responds preferentially to emotionally valenced faces and rapidly habituates to them.

Categorical perception of facial expressions.

People universally recognize facial expressions of happiness, sadness, fear, anger, disgust, and perhaps, surprise, suggesting a perceptual mechanism tuned to the facial configuration displaying each emotion. Sets of drawings were generated by computer, each consisting of a series of faces differing by constant physical amounts, running from one emotional expression to another (or from one emotional expression to a neutral face). Subjects discriminated pairs of faces, then, in a separate task, categorized the emotion displayed by each. Faces within a category were discriminated more poorly than faces in different categories that differed by an equal physical amount. Thus emotional expressions, like colors and speech sounds, are perceived categorically, not as a direct reflection of their continuous physical properties.

Can we lose memories of faces? Content specificity and awareness in a prosopagnosic.

Prosopagnosia is a neurological syndrome in which patients cannot recognize faces. Kecently it has been shown that some prosopagnosics give evidence of "covert" recognition: they show greater autonomic responses to familiar faces than to unfamiliar ones, and respond differently to familiar faces in learning and interference tasks. Although some patients do not show covert recognition, this has usually been attributed to an "apperceptive" deficit that impairs perceptual analysis of the input. The implication is that prosopagnosia is a deficit in access to, or awareness of, memories of faces: the inducing brain injury does not destroy the memories themselves. We present a case study that challenges this view. LH suffers from prosopagnosia as the result of a closed head injury. He cannot recognize familiar faces or report that they are familiar, nor answer questions about the faces from memory, though he can (1) recognize common objects and subtly varying shapes, (2) match faces while ignoring irrelevant information such as emotional expression or angle of view, (3) recognize sex, age, and like-ability from faces, and (4) recognize people by a number of nonfacial channels. The only other categories of shapes that he has marked trouble recognizing are animals and emotional expressions, though even these impairments were not as severe as the one for faces. Three measures (sympathetic skin response, pupil dilation, and learning correct and incorrect names of faces) failed to show any signs of covert face recognition in LH, though the measures were sensitive enough to reflect autonomic reactions in LH to stimuli other than faces, and face familiarity in normal controls. Thus prosopagnosia cannot always be attributed to a mere absence of awareness (i.e., preserved information about faces whose output is disconnected from conscious cognitive processing), to an apperceptive deficit (i.e., preserved information about faces that cannot be accessed due to improperly analyzed perceptual input), or to an inability to recognize complex or subtly varying shapes (i.e., loss or degradation of shape memory in general). We conclude that it is possible for brain injury to eliminate the storage of information about familiar faces and certain related shapes.

Perceptual and conceptual organization of facial emotions: hemispheric differences.

Patients with lesions to either the right or left hemisphere and control subjects were asked to judge the similarity of pairs of photographs of a person displaying different emotions, and of pairs of emotion words. The results were submitted to a multidimensional scaling analysis. Right-hemisphere-damaged subjects were found to be more impaired at perceiving facial emotions than were left-hemisphere-damaged subjects or controls, and this impairment was not confined to the perception of a subset of facial emotions nor to judging emotional valence (Pleasantness versus Unpleasantness). Rather, subtle impairments in perceiving a wide range of facial emotions were found, mostly concerning differentiation of the Positive-Negative and Attention-Rejection dimensions, and concerning the strategies the subjects used to make their judgments. The right-hemisphere-damaged subjects performed comparably to controls in their ratings of emotion words, suggesting that their ability to conceptualize emotional states was intact and that their impairment was strictly in the perception of emotion.

Selective attention to facial identity and facial emotion.

Patients with lesions to either the right or left hemisphere and control subjects were asked to discriminate photographs of faces and then to sort these photographs according to the identity of the face or the emotion displayed. Whether identity and emotion were correlated, independent, or constant was varied across trials. Patients with right hemisphere damage were significantly impaired at discriminating both identity and expression, and at selectively attending to either sort of facial information. However, these subjects could selectively attend to attributes of geometric figures suggesting that their impairment with faces cannot be attributed to deficits in selective attention in general.