The perception of positive and negative facial expressions in unilateral brain-damaged patients: A meta-analysis

How the brain is lateralised for emotion processing remains a key question in contemporary neuropsychological research. The right hemisphere hypothesis asserts that the right hemisphere dominates emotion processing, whereas the valence hypothesis holds that positive emotion is processed in the left hemisphere and negative emotion is controlled by the right hemisphere. A meta-analysis was conducted to assess unilateral brain-damaged individuals’ performance on tasks of facial emotion perception according to valence. A systematic search of the literature identified seven articles that met the conservative selection criteria and could be included in a meta-analysis. A total of 12 meta-analyses of facial expression perception were constructed assessing identification and labelling tasks according to valence and the side of brain damage. The results demonstrated that both left and right hemisphere damage leads to impairments in emotion perception (identification and labelling) irrespective of valence. Importantly, right hemisphere damage prompted more pronounced emotion perception impairment than left hemisphere damage, across valence, suggesting right hemisphere dominance for emotion perception. Furthermore, right hemisphere damage was associated with a larger tendency for impaired perception of negative than positive emotion across identification and labelling tasks. Overall the findings support Adolphs, Jansari, and Tranel (2001) model whereby the right hemisphere preferentially processes negative facial expressions and both hemispheres process positive facial expressions.     

Facial recognition 1990

A review of recent studies of prosopagnosia suggests that the weight of evidence has shifted in favor of regarding it as a disability that can be produced by a right hemisphere lesion alone even though bilateral disease remains the more frequent anatomical basis. It is possible that prosopagnosia resulting from a right hemisphere lesion occurs only within the context of some atypical condition of the left hemisphere. "Types" of prosopagnosia continue to be postulated and the "identification of individuality" hypothesis continues to be advanced. Autonomic and covert recognition studies of prosopagnosic patients have described a new dimension in facial identification. Right hemisphere dominance for the discrimination of unfamiliar faces in non-aphasic patients has been confirmed but the performances of left-hemisphere damaged aphasic patients has still not been fully investigated. New developments include the study of developmental prosopagnosia and novel applications of test of facial discrimination.     

Selective impairment of facial recognition due to a haematoma restricted to the right fusiform and lateral occipital region

A 67 year old right handed Japanese man developed prosopagnosia caused by a haemorrhage. His only deficit was the inability to perceive and discriminate unfamiliar faces, and to recognise familiar faces. He did not show deficits in visual or visuospatial perception of non-facial stimuli, alexia, visual agnosia, or topographical disorientation. Brain MRI showed a haematoma limited to the right fusiform and the lateral occipital region. Single photon emission computed tomography confirmed that there was no decreased blood flow in the opposite left cerebral hemisphere. The present case indicates that a well placed small right fusiform gyrus and the adjacent area can cause isolated impairment of facial recognition. As far as we know, there has been no published case that has demonstrated this exact lesion site, which was indicated by recent functional MRI studies as the most critical area in facial recognition.     

Representations of facial identity in the left hemisphere require right hemisphere processing

A quintessential example of hemispheric specialization in the human brain is that the right hemisphere is specialized for face perception. However, because the visual system is organized contralaterally, what happens when faces appear in the right visual field and are projected to the nonspecialized left hemisphere? We used divided field presentation and fMRI adaptation to test the hypothesis that the left hemisphere can recognize faces, but only with support from the right hemisphere. Consistent with this hypothesis, facial identity adaptation was observed in the left fusiform face area when a face had previously been processed by the right hemisphere, but not when it had only been processed by the left hemisphere. These results imply that facial identity information is transferred from the right hemisphere to the left hemisphere, and that the left hemisphere can represent facial identity but is less efficient at extracting this information by itself.     

Right cerebral hemisphere superiority for constructing facial representations

Right-handed people were asked to decide whether or not stimuli presented in the left visual hemifield (LVF) or in the right visual hemifield (RVF) were faces. Manual reaction times and error rates were recorded under three conditions. In Condition A, stimuli were line drawings of faces and moderately scrambled nonfaces made by rearranging the facial features. In Condition B, stimuli were line drawings of faces and highly scrambled nonfaces. In Condition C, stimuli were line drawings of faces and objects. The results show that faces are identified more quickly from the LVF than from the RVF in Condition A (faces vs moderately scrambled nonfaces), with no visual hemifield difference in reaction times to Condition B (faces vs highly scrambled nonfaces) and Condition C (faces vs objects). These findings are taken to indicate that both cerebral hemispheres are able to assign stimuli to the "face" category, but the right hemisphere is better than the left hemisphere at constructing facial representations. This cerebral hemisphere difference in ability to construct facial representations becomes evident when a detailed representation is required (as in Condition A).     

Neural correlates of the left-visual-field superiority in face perception appear at multiple stages of face processing

Studies in healthy individuals and split-brain patients have shown that the representation of facial information from the left visual field (LVF) is better than the representation of facial information from the right visual field (RVF). To investigate the neurophysiological basis of this LVF superiority in face perception, we recorded event-related potentials (ERPs) to centrally presented face stimuli in which relevant facial information is present bilaterally (B faces) or only in the left (L faces) or the right (R faces) visual field. Behavioral findings showed best performance for B faces and, in line with the LVF superiority, better performance for L than R faces. Evoked potentials to B, L, and R faces at 100- to 150-msec poststimulus showed no evidence of asymmetric transfer of information between the hemispheres at early stages of visual processing, suggesting that this factor is not responsible for the LVF superiority. Neural correlates of the LVF superiority, however, were manifested in a shorter latency of the face-specific N170 component to L than R faces and in a larger amplitude to L than R faces at 220-280 and 400-600 msec over both hemispheres. These ERP amplitude differences between L and R faces covaried across subjects with the extent to which the face-specific N170 component was larger over the right than the left hemisphere. We conclude that the two hemispheres exchange information symmetrically at early stages of face processing and together generate a shared facial representation, which is better when facial information is directly presented to the right hemisphere (RH; L faces) than to the left hemisphere (LH; R faces) and best when both hemispheres receive facial information (B faces).     

A functional MRI study of face recognition in patients with prosopagnosia.

An fMRI investigation was conducted to determine whether patients with impaired face recognition, a deficit known as prosopagnosia, would show functional activation in the fusiform gyrus, the neural substrate for face processing, when viewing faces. While the patients did show activation in the fusiform gyrus, with significantly more voxels in posterior areas than their control subjects, this activation was not sufficient for face processing. In one of the patients, the posterior activation was particularly evident in the left hemisphere, which is thought to be involved in feature-based strategies of face perception. We conclude that an increased reliance on feature-based processing in prosopagnosia leads to a recruitment of neurons in posterior regions of the fusiform gyrus, regions that are not ideally suited for processing faces.     

Holistic perception of the individual face is specific and necessary: Evidence from an extensive case study of acquired prosopagnosia

We present an extensive investigation (24 experiments) of a new case of prosopagnosia following right unilateral damage, GG, with the aim of addressing two classical issues: (1) Can a visual recognition impairment truly be specific to faces? (2) What is the nature of acquired prosopagnosia? We show that GG recognizes nonface objects perfectly and quickly, even when it requires fine-grained analysis to individualize these objects. He is also capable of perceiving objects and faces as integrated wholes, as indicated by normal Navon effect, 3D-figures perception and perception of Mooney and Arcimboldo face stimuli. However, the patient could not perceive individual faces holistically, showing no inversion, composite, or whole-part advantage effects for faces. We conclude that an occipito-temporal right hemisphere lesion may lead to a specific impairment of holistic perception of individual items, a function that appears critical for normal face recognition but not for object recognition.     

Cerebral lateralization of face-sensitive areas in left-handers: Only the FFA does not get it right

Face perception is highly lateralized to the right hemisphere (RH) in humans, as supported originally by observations of face recognition impairment (prosopagnosia) following brain damage. Divided visual field presentations, neuroimaging and event-related potential studies have supported this view. While the latter studies are typically performed in right-handers, the few reported cases of prosopagnosia with unilateral left damage were left-handers, suggesting that handedness may shift or qualify the lateralization of face perception. We tested this hypothesis by recording the whole set of face-sensitive areas in 11 left-handers, using a face-localizer paradigm in functional magnetic resonance imaging (fMRI) (faces, cars, and their phase-scrambled versions). All face-sensitive areas identified (superior temporal sulcus, inferior occipital cortex, anterior infero-temporal cortex, amygdala) were strongly right-lateralized in left-handers, this right lateralization bias being as large as in a population of right-handers (40) tested with the same paradigm (Rossion et al., 2012). The notable exception was the so-called ‘Fusiform face area’ (FFA), an area that was slightly left lateralized in the population of left-handers. Since the left FFA is localized closely to an area sensitive to word form in the human brain (‘Visual Word Form Area’ – VWFA), the enhanced left lateralization of the FFA in left-handers may be due to a decreased competition with the representation of words. The implications for the neural basis of face perception, aetiology of brain lateralization in general, and prosopagnosia are also discussed.     

Perception of emotions from faces and voices following unilateral brain damage

The importance of the right hemisphere in emotion perception in general has been well documented but its precise role is disputed. We compared the performance of 30 right hemisphere damaged (RHD) patients, 30 left hemisphere damaged (LHD) patients, and 50 healthy controls on both facial and vocal affect perception tasks of specific emotions. Brain damaged subjects had a single episode cerebrovascular accident localised to one hemisphere. The results showed that right hemisphere patients were markedly impaired relative to left hemisphere and healthy controls on test performance: labelling and recognition of facial expressions and recognition of emotions conveyed by prosody. This pertained at the level of individual basic emotions, positive versus negative, and emotional expressions in general. The impairment remained highly significant despite covarying for the group's poorer accuracy on a neutral facial perception test and identification of neutral vocal expressions. The LHD group were only impaired relative to controls on facial emotion tasks when their performance was summed over all the emotion categories and before age and other cognitive factors were taken into account. However, on the prosody test the LHD patients showed significant impairment, performing mid-way between the right hemisphere patients and healthy comparison group. Recognition of positive emotional expressions was better than negative in all subjects, and was not relatively poorer in the LHD patients. Recognition of individual emotions in one modality correlated weakly with recognition in another, in all three groups. These data confirm the primacy of the right hemisphere in processing all emotional expressions across modalities--both positive and negative--but suggest that left hemisphere emotion processing is modality specific. It is possible that the left hemisphere has a particular role in the perception of emotion conveyed through meaningful speech.     

Patterns of brain asymmetry in the perception of positive and negative facial expressions

The divided visual field technique was used to investigate the pattern of brain asymmetry in the perception of positive/approach and negative/withdrawal facial expressions. A total of 80 undergraduate students (65 female, 15 male) were distributed in five experimental groups in order to investigate separately the perception of expressions of happiness, surprise, fear, sadness, and the neutral face. In each trial a target and a distractor expression were presented simultaneously in a computer screen for 150 ms and participants had to determine the side (left or right) on which the target expression was presented. Results indicated that expressions of happiness and fear were identified faster when presented in the left visual field, suggesting an advantage of the right hemisphere in the perception of these expressions. Fewer judgement errors and faster reaction times were also observed for the matching condition in which emotional faces were presented in the left visual field and neutral faces in the right visual field. Other results indicated that positive expressions (happiness and surprise) were perceived faster and more accurately than negative ones (sadness and fear). Main results tend to support the right hemisphere hypothesis, which predicts a better performance of the right hemisphere to perceive emotions, as opposed to the approach–withdrawal hypothesis.     

Prosopagnosia as a deficit in encoding curved surface

RP is a case of "developmental" prosopagnosia who, according to brain-imaging segmentation data, shows reduction in volume of a limited set of structures of the right hemisphere. RP is as accurate as control subjects in tasks requiring the perception of nonface objects (e.g., matching subordinate labels to exemplars, naming two-tone images), with the exception of one perceptual task: The matching of different perspectives of amoebae-like stimuli (i.e., volumes made of a single smooth surface). In terms of speed ("efficiency") of responses, RP's performance falls clearly outside the normal limits also in other tasks that include "natural" but nonface stimuli (i.e., animals, artia facts). Specifically, RP is slow in perceptual judgments made at very low (subordinate) levels of semantic categorization and for objects and artifacts whose geometry present much curved features and surface information. We conclude from these analyses that prosopagnosia can be the result of a deficit in the representation of basic geometric volumes made of curved surface. In turn, this points to the importance (necessity) for the normal visual system of such curved and volumetric information in the identification of human faces.     

Patterns of brain asymmetry in the perception of positive and negative facial expressions

The divided visual field technique was used to investigate the pattern of brain asymmetry in the perception of positive/approach and negative/withdrawal facial expressions. A total of 80 undergraduate students (65 female, 15 male) were distributed in five experimental groups in order to investigate separately the perception of expressions of happiness, surprise, fear, sadness, and the neutral face. In each trial a target and a distractor expression were presented simultaneously in a computer screen for 150 ms and participants had to determine the side (left or right) on which the target expression was presented. Results indicated that expressions of happiness and fear were identified faster when presented in the left visual field, suggesting an advantage of the right hemisphere in the perception of these expressions. Fewer judgement errors and faster reaction times were also observed for the matching condition in which emotional faces were presented in the left visual field and neutral faces in the right visual field. Other results indicated that positive expressions (happiness and surprise) were perceived faster and more accurately than negative ones (sadness and fear). Main results tend to support the right hemisphere hypothesis, which predicts a better performance of the right hemisphere to perceive emotions, as opposed to the approach-withdrawal hypothesis.     

Impairment of holistic face perception following right occipito-temporal damage in prosopagnosia: converging evidence from gaze-contingency

Gaze-contingency is a method traditionally used to investigate the perceptual span in reading by selectively revealing/masking a portion of the visual field in real time. Introducing this approach in face perception research showed that the performance pattern of a brain-damaged patient with acquired prosopagnosia (PS) in a face matching task was reversed, as compared to normal observers: the patient showed almost no further decrease of performance when only one facial part (eye, mouth, nose, etc.) was available at a time (foveal window condition, forcing part-based analysis), but a very large impairment when the fixated part was selectively masked (mask condition, promoting holistic perception) ( [Van Belle et al., 2010a] and [Van Belle et al., 2010b] ). Here we tested the same manipulation in a recently reported case of pure prosopagnosia (GG) with unilateral right hemisphere damage (Busigny, Joubert, Felician, Ceccaldi, & Rossion, 2010). Contrary to normal observers, GG was also significantly more impaired with a mask than with a window, demonstrating impairment with holistic face perception. Together with our previous study, these observations support a generalized account of acquired prosopagnosia as a critical impairment of holistic (individual) face perception, implying that this function is a key element of normal human face recognition. Furthermore, the similar behavioral pattern of the two patients despite different lesion localizations supports a distributed network view of the neural face processing structures, suggesting that the key function of human face processing, namely holistic perception of individual faces, requires the activity of several brain areas of the right hemisphere and their mutual connectivity.     

Lateralised repetition priming for featurally and configurally manipulated familiar faces: evidence for differentially lateralised processing mechanisms

Although early research suggested that the right hemisphere was dominant for processing faces, more recent studies have provided evidence for both hemispheres being involved, at least to some extent. In this experiment we examined hemispheric specialisations by using a lateralised repetition-priming paradigm with selectively degraded faces. Configurally degraded prime faces produced negative priming when presented to the left visual field (right hemisphere) and positive priming (facilitation) when presented to the right visual field (left hemisphere). Featurally degraded prime faces produced the opposite pattern of effects: positive priming when presented to the left visual field (right hemisphere) and negative priming when presented to the right visual field (left hemisphere). These results support the proposal that each hemisphere is differentially specialised for processing distinct forms of facial information: the right hemisphere for configural information and the left hemisphere for featural information.     

Laterality Biases to Chimeric Faces in Asperger Syndrome: What is Right About Face-Processing?

People show a left visual field (LVF) bias for faces, i.e., involving the right hemisphere of the brain. Lesion and neuroimaging studies confirm the importance of the right-hemisphere and suggest separable neural pathways for processing facial identity vs. emotions. We investigated the hemispheric processing of faces in adults with and without Asperger syndrome (AS) using facial emotion and identity chimeric tasks. Controls showed an LVF bias in both tasks, but no perceptual bias in a non-social control task. The AS group showed an LVF bias during both tasks, however the bias was reduced in the identity condition. Further, the AS group showed an LVF bias in the non-social condition. These results show a differential pattern of hemispheric processing of faces in AS.     

Asymmetry of visual perceptive activity of faces and emotional facial expressions

Eye movements were studied in 40 right-handed subjects during perception of symmetrical chimerical faces. These movements were recorded using an original system based on a differential optical method for the detection of corneal reflection and of the pupil made shiny. Under basal conditions, the first fixation was usually located in the left visual hemifield. The subjects spent more time gazing at the right hemiface (P less than 0.04). This visuo-spatial asymmetry in favour of the left hemispace was increased when the subject was requested to determine the emotional expressions of a new series of faces (P less than 0.002). Compared with basal conditions, the increase in the percentage of time spent in the left area was significant (P less than 0.035). An analysis performed on the first 3 seconds confirmed and amplified the differences observed. These results can partly be explained by reading habits and exploratory activity for symmetrical shapes. However, activation of the right hemisphere, specialized in the perception of faces and facial expressions, probably influenced visual exploration by drawing attention to the left area and favouring the left visual hemifield.     

Evidence of interhemispheric transmission in laterality effects

The study was aimed at testing various models that can explain visual lateral asymmetries due to hemispheric specialization. In Experiments 1-3 the subjects had to perform a lateralized "go-no go" discrimination of words (primary task) either alone or in association with secondary tasks that interfered with the processing of the left hemisphere (ordered tapping) or the right hemisphere (finger flexion). In Experiment 4 the primary task was one of lateralized "go-no go" discrimination of faces while the secondary tasks were again those of ordered tapping and finger flexion. The results showed that in the case of word discrimination the advantage in speed of response in favour of the right visual field/left hemisphere (RVF/LH), which was observed for the primary task alone, did not change when the secondary task was added. This held true irrespective of whether the secondary task loaded the left or right hemisphere. The advantage for the left visual field/right hemisphere (LVF/RH) observed for face discrimination alone, disappeared when the secondary task interfered with the processing of the right hemisphere and did not change when the secondary task concerned the left hemisphere. It was concluded that each hemisphere is able to elaborate in parallel the incoming information, but, in normal conditions, interhemispheric transmission is responsible for the lateral asymmetries in perception (conditional interhemispheric transmission model).     

False recognition of faces associated with fronto-temporal dementia with prosopagnosia

INTRODUCTION: The association of prosopagnosia and false recognition of faces is unusual and contributes to our understanding of the generation of facial familiarity. METHOD: A 67-year-old man with a left prefrontal traumatic lesion, developed a temporal variety of fronto-temporal dementia (semantic dementia) with amyotrophic lateral sclerosis. Cerebral imagery demonstrated a bilateral, temporal anterior atrophy predominating in the right hemisphere. The main cognitive signs consisted in severe difficulties to recognize faces of familiar people (prosopagnosia), associated with systematic false recognition of unfamiliar people. RESULT: Neuropsychological testing indicated that the prosopagnosia probably resulted from the association of an associative/mnemonic mechanism (inability to activate the Face Recognition Units (FRU) from the visual input) and a semantic mechanism (degradation of semantic/biographical information or deconnexion between FRU and this information). At the early stage of the disease, the patient could activate residual semantic information about individuals from their names, but after a 4-year course, he failed to do so. This worsening could be attributed to the extension of the degenerative lesions to the left temporal lobe. Familiar and unfamiliar faces triggered a marked feeling of knowing. False recognition concerned all the unfamiliar faces, and the patient claimed spontaneously that they corresponded to actors, but he could not provide any additional information about their specific identities. The coexistence of prosopagnosia and false recognition suggests the existence of different interconnected systems processing face recognition, one intended to identification of individuals, and the other producing the sense of familiarity. Dysfunctions at different stages of one or the other of these two processes could result in distortions in the feeling of knowing. CONCLUSION: From this case and others reported in literature, we propose to complete the classical model of face processing by adding a pathway linked to limbic system and frontal structures. This later pathway could normally emit signals for familiarity, essentially autonomic, in response to the familiar faces. These signals, primitively unconscious, secondly reach consciousness and are then integrated by a central supervisor system which evaluates and verifies identity-specific biographical information in order to make a decision about the sense of familiarity.