The Background of Reduced Face Specificity of N170 in Congenital Prosopagnosia

Congenital prosopagnosia is lifelong face-recognition impairment in the absence of evidence for structural brain damage. To study the neural correlates of congenital prosopagnosia, we measured the face-sensitive N170 component of the event-related potential in three members of the same family (father (56 y), son (25 y) and daughter (22 y)) and in age-matched neurotypical participants (young controls: n = 14; 24.5 y±2.1; old controls: n = 6; 57.3 y±5.4). To compare the face sensitivity of N170 in congenital prosopagnosic and neurotypical participants we measured the event-related potentials for faces and phase-scrambled random noise stimuli. In neurotypicals we found significantly larger N170 amplitude for faces compared to noise stimuli, reflecting normal early face processing. The congenital prosopagnosic participants, by contrast, showed reduced face sensitivity of the N170, and this was due to a larger than normal noise-elicited N170, rather than to a smaller face-elicited N170. Interestingly, single-trial analysis revealed that the lack of face sensitivity in congenital prosopagnosia is related to a larger oscillatory power and phase-locking in the theta frequency-band (4–7 Hz, 130–190 ms) as well as to a lower intertrial jitter of the response latency for the noise stimuli. Altogether, these results suggest that congenital prosopagnosia is due to the deficit of early, structural encoding steps of face perception in filtering between face and non-face stimuli.     

The role of gamma-band activity in the representation of faces: reduced activity in the fusiform face area in congenital prosopagnosia

Background

Congenital prosopagnosia (CP) describes an impairment in face processing that is presumably present from birth. The neuronal correlates of this dysfunction are still under debate. In the current paper, we investigate high-frequent oscillatory activity in response to faces in persons with CP. Such neuronal activity is thought to reflect higher-level representations for faces.

Methodology

Source localization of induced Gamma-Band Responses (iGBR) measured by magnetoencephalography (MEG) was used to establish the origin of oscillatory activity in response to famous and unknown faces which were presented in upright and inverted orientation. Persons suffering from congenital prosopagnosia (CP) were compared to matched controls.

Principal Findings

Corroborating earlier research, both groups revealed amplified iGBR in response to upright compared to inverted faces predominately in a time interval between 170 and 330 ms and in a frequency range from 50–100 Hz. Oscillatory activity upon known faces was smaller in comparison to unknown faces, suggesting a “sharpening” effect reflecting more efficient processing for familiar stimuli. These effects were seen in a wide cortical network encompassing temporal and parietal areas involved in the disambiguation of homogenous stimuli such as faces, and in the retrieval of semantic information. Importantly, participants suffering from CP displayed a strongly reduced iGBR in the left fusiform area compared to control participants.

Conclusions

In sum, these data stress the crucial role of oscillatory activity for face representation and demonstrate the involvement of a distributed occipito-temporo-parietal network in generating iGBR. This study also provides the first evidence that persons suffering from an agnosia actually display reduced gamma band activity. Finally, the results argue strongly against the view that oscillatory activity is a mere epiphenomenon brought fourth by rapid eye-movements (micro saccades).     

The Early Time Course of Compensatory Face Processing in Congenital Prosopagnosia

Background

Prosopagnosia is a selective deficit in facial identification which can be either acquired, (e.g., after brain damage), or present from birth (congenital). The face recognition deficit in prosopagnosia is characterized by worse accuracy, longer reaction times, more dispersed gaze behavior and a strong reliance on featural processing.

Methods/Principal Findings

We introduce a conceptual model of an apperceptive/associative type of congenital prosopagnosia where a deficit in holistic processing is compensated by a serial inspection of isolated, informative features. Based on the model proposed we investigated performance differences in different face and shoe identification tasks between a group of 16 participants with congenital prosopagnosia and a group of 36 age-matched controls. Given enough training and unlimited stimulus presentation prosopagnosics achieved normal face identification accuracy evincing longer reaction times. The latter increase was paralleled by an equally-sized increase in stimulus presentation times needed achieve an accuracy of 80%. When the inspection time of stimuli was limited (50ms to 750ms), prosopagnosics only showed worse accuracy but no difference in reaction time. Tested for the ability to generalize from frontal to rotated views, prosopagnosics performed worse than controls across all rotation angles but the magnitude of the deficit didn''t change with increasing rotation. All group differences in accuracy, reaction or presentation times were selective to face stimuli and didn''t extend to shoes.

Conclusions/Significance

Our study provides a characterization of congenital prosopagnosia in terms of early processing differences. More specifically, compensatory processing in congenital prosopagnosia requires an inspection of faces that is sufficiently long to allow for sequential focusing on informative features. This characterization of dysfunctional processing in prosopagnosia further emphasizes fast and holistic information encoding as two defining characteristics of normal face processing.     

The effect of face inversion on activity in human neural systems for face and object perception

The differential effect of stimulus inversion on face and object recognition suggests that inverted faces are processed by mechanisms for the perception of other objects rather than by face perception mechanisms. We investigated the face inversion using functional magnetic resonance imaging (fMRI). The principal effect of face inversion on was an increased response in ventral extrastriate regions that respond preferentially to another class of objects (houses). In contrast, house inversion did not produce a similar change in face-selective regions. Moreover, stimulus inversion had equivalent, minimal effects for faces in in face-selective regions and for houses in house-selective regions. The results suggest that the failure of face perception systems with inverted faces leads to the recruitment of processing resources in object perception systems, but this failure is not reflected by altered activity in face perception systems.     

Gender difference in N170 elicited under oddball task

Background

Some studies have reported gender differences in N170, a face-selective event-related potential (ERP) component. This study investigated gender differences in N170 elicited under oddball paradigm in order to clarify the effect of task demand on gender differences in early facial processing.

Findings

Twelve males and 10 females discriminated targets (emotional faces) from non-targets (emotionally neutral faces) under an oddball paradigm, pressing a button as quickly as possible in response to the target. Clear N170 was elicited in response to target and non-target stimuli in both males and females. However, females showed more negative amplitude of N170 in response to target compared with non-target, while males did not show different N170 responses between target and non-target.

Conclusions

The present results suggest that females have a characteristic of allocating attention at an early stage when responding to faces actively (target) compared to viewing faces passively (non-target). This supports previous findings suggesting that task demand is an important factor in gender differences in N170.     

Impairments of Biological Motion Perception in Congenital Prosopagnosia

Prosopagnosia is a deficit in recognizing people from their faces. Acquired prosopagnosia results after brain damage, developmental or congenital prosopagnosia (CP) is not caused by brain lesion, but has presumably been present from early childhood onwards. Since other sensory, perceptual, and cognitive abilities are largely spared, CP is considered to be a stimulus-specific deficit, limited to face processing. Given that recent behavioral and imaging studies indicate a close relationship of face and biological-motion perception in healthy adults, we hypothesized that biological motion processing should be impaired in CP. Five individuals with CP and ten matched healthy controls were tested with diverse biological-motion stimuli and tasks. Four of the CP individuals showed severe deficits in biological-motion processing, while one performed within the lower range of the controls. A discriminant analysis classified all participants correctly with a very high probability for each participant. These findings demonstrate that in CP, impaired perception of faces can be accompanied by impaired biological-motion perception. We discuss implications for dedicated and shared mechanisms involved in the perception of faces and biological motion.     

The naked truth: the face and body sensitive N170 response is enhanced for nude bodies

Recent event-related potential studies have shown that the occipitotemporal N170 component--best known for its sensitivity to faces--is also sensitive to perception of human bodies. Considering that in the timescale of evolution clothing is a relatively new invention that hides the bodily features relevant for sexual selection and arousal, we investigated whether the early N170 brain response would be enhanced to nude over clothed bodies. In two experiments, we measured N170 responses to nude bodies, bodies wearing swimsuits, clothed bodies, faces, and control stimuli (cars). We found that the N170 amplitude was larger to opposite and same-sex nude vs. clothed bodies. Moreover, the N170 amplitude increased linearly as the amount of clothing decreased from full clothing via swimsuits to nude bodies. Strikingly, the N170 response to nude bodies was even greater than that to faces, and the N170 amplitude to bodies was independent of whether the face of the bodies was visible or not. All human stimuli evoked greater N170 responses than did the control stimulus. Autonomic measurements and self-evaluations showed that nude bodies were affectively more arousing compared to the other stimulus categories. We conclude that the early visual processing of human bodies is sensitive to the visibility of the sex-related features of human bodies and that the visual processing of other people's nude bodies is enhanced in the brain. This enhancement is likely to reflect affective arousal elicited by nude bodies. Such facilitated visual processing of other people's nude bodies is possibly beneficial in identifying potential mating partners and competitors, and for triggering sexual behavior.     

Deficits in long-term recognition memory reveal dissociated subtypes in congenital prosopagnosia

The study investigates long-term recognition memory in congenital prosopagnosia (CP), a lifelong impairment in face identification that is present from birth. Previous investigations of processing deficits in CP have mostly relied on short-term recognition tests to estimate the scope and severity of individual deficits. We firstly report on a controlled test of long-term (one year) recognition memory for faces and objects conducted with a large group of participants with CP. Long-term recognition memory is significantly impaired in eight CP participants (CPs). In all but one case, this deficit was selective to faces and didn't extend to intra-class recognition of object stimuli. In a test of famous face recognition, long-term recognition deficits were less pronounced, even after accounting for differences in media consumption between controls and CPs. Secondly, we combined test results on long-term and short-term recognition of faces and objects, and found a large heterogeneity in severity and scope of individual deficits. Analysis of the observed heterogeneity revealed a dissociation of CP into subtypes with a homogeneous phenotypical profile. Thirdly, we found that among CPs self-assessment of real-life difficulties, based on a standardized questionnaire, and experimentally assessed face recognition deficits are strongly correlated. Our results demonstrate that controlled tests of long-term recognition memory are needed to fully assess face recognition deficits in CP. Based on controlled and comprehensive experimental testing, CP can be dissociated into subtypes with a homogeneous phenotypical profile. The CP subtypes identified align with those found in prosopagnosia caused by cortical lesions; they can be interpreted with respect to a hierarchical neural system for face perception.     

Functional and anatomical decomposition of face processing: evidence from prosopagnosia and PET study of normal subjects.

Studies of brain-damaged patients have revealed the existence of a selective impairment of face processing, prosopagnosia, resulting from lesions at different loci in the occipital and temporal lobes. The lesions are often extensive, and it is unclear what functional aspects of face processing are normally served by the damaged areas, and whether they are uniquely devoted to the processing of faces. These issues are further addressed through a combined magnetic resonance imaging (MRI) and positron emission tomography (PET) study of regional cerebral blood flow (rCBF) in normal subjects performing different tasks of face and object processing. The results indicate different patterns of cerebral activation depending on the requirements of the tasks within the processing of faces, as well as a clear dissociation of the neural substrates underlying face and object processing. These results are compared with radiological data from prosopagnosic patients, and are put in relation with the patterns of deficits observed in the patients as a function of the location of their lesions. Together, the findings offer new evidence regarding the functional neuroanatomy of face and object processing.     

The neural basis of the behavioral face-inversion effect

Two of the most robust markers for "special" face processing are the behavioral face-inversion effect (FIE)-the disproportionate drop in recognition of upside-down (inverted) stimuli relative to upright faces-and the face-selective fMRI response in the fusiform face area (FFA). However, the relationship between these two face-selective markers is unknown. Here we report that the behavioral FIE is closely associated with the fMRI response in the FFA, but not in other face-selective or object-selective regions. The FFA and the face-selective region in the superior temporal sulcus (f_STS), but not the occipital face-selective region (OFA), showed a higher response to upright than inverted faces. However, only in the FFA was this fMRI-FIE positively correlated across subjects with the behavioral FIE. Second, the FFA, but not the f_STS, showed greater neural sensitivity to differences between faces when they were upright than inverted, suggesting a possible neural mechanism for the behavioral FIE. Although a similar trend was found in the occipital face area (OFA), it was less robust than the FFA. Taken together, our data suggest that among the face-selective and object-selective regions, the FFA is a primary neural source of the behavioral FIE.     

Mind perception: real but not artificial faces sustain neural activity beyond the N170/VPP

Faces are visual objects that hold special significance as the icons of other minds. Previous researchers using event-related potentials (ERPs) have found that faces are uniquely associated with an increased N170/vertex positive potential (VPP) and a more sustained frontal positivity. Here, we examined the processing of faces as objects vs. faces as cues to minds by contrasting images of faces possessing minds (human faces), faces lacking minds (doll faces), and non-face objects (i.e., clocks). Although both doll and human faces were associated with an increased N170/VPP from 175-200 ms following stimulus onset, only human faces were associated with a sustained positivity beyond 400 ms. Our data suggest that the N170/VPP reflects the object-based processing of faces, whether of dolls or humans; on the other hand, the later positivity appears to uniquely index the processing of human faces--which are more salient and convey information about identity and the presence of other minds.     

Effect of empathy trait on attention to various facial expressions: evidence from N170 and late positive potential (LPP)

Background

The present study sought to clarify the relationship between empathy trait and attention responses to happy, angry, surprised, afraid, and sad facial expressions. As indices of attention, we recorded event-related potentials (ERP) and focused on N170 and late positive potential (LPP) components.

Methods

Twenty-two participants (12 males, 10 females) discriminated facial expressions (happy, angry, surprised, afraid, and sad) from emotionally neutral faces under an oddball paradigm. The empathy trait of participants was measured using the Interpersonal Reactivity Index (IRI, J Pers Soc Psychol 44:113–126, 1983).

Results

Participants with higher IRI scores showed: 1) more negative amplitude of N170 (140 to 200 ms) in the right posterior temporal area elicited by happy, angry, surprised, and afraid faces; 2) more positive amplitude of early LPP (300 to 600 ms) in the parietal area elicited in response to angry and afraid faces; and 3) more positive amplitude of late LPP (600 to 800 ms) in the frontal area elicited in response to happy, angry, surprised, afraid, and sad faces, compared to participants with lower IRI scores.

Conclusions

These results suggest that individuals with high empathy pay attention to various facial expressions more than those with low empathy, from very-early stage (reflected in N170) to late-stage (reflected in LPP) processing of faces.     

Visual evoked potentials in a patient with prosopagnosia

Visual evoked potentials (VEPs) were recorded from a 53-year-old man with prosopagnosia during presentation of slides of known and unknown faces and under two control conditions. ANOVA comparisons with a normal male group showed no differences in P100 amplitude, P300 amplitude or P300 latency. There were no significant evoked potential differences between the patient and controls specifically related to the face conditions.There was, however, a significant delay in the latency of P100 from both hemispheres during all types of stimuli. This prolonged latency was asymmetrical, showing a right sided emphasis with the control conditions: pattern reversal and slides of geometric designs. This finding, of a dissociation in the interhemispheric delay, provides physiological evidence of stimulus-specific organisation at an early, sensory level.The fact that the P100 component showed a marked delay, yet P300 fell within normal limits for amplitude and latency, suggests that this patient's problem lies at a perceptual level.     

Stimulation of category-selective brain areas modulates ERP to their preferred categories

Neural selectivity to specific object categories has been demonstrated in extrastriate cortex with both functional MRI [1-3] and event-related potential (ERP) [4, 5]. Here we tested for a causal relationship between the activation of category-selective areas and ERP to their preferred categories. Electroencephalogram (EEG) was recorded while participants observed faces and headless bodies. Concurrently with EEG recording, we delivered two pulses of transcranial magnetic stimulation (TMS) over the right occipital face area (OFA) or extrastriate body area (EBA) at 60 and 100 ms after stimulus onset. Results showed a clear dissociation between the stimulated site and the stimulus category on ERP modulation: stimulation of the OFA significantly increased the N1 amplitude to faces but not to bodies, whereas stimulation of the EBA significantly increased the N1 amplitude to bodies but not to faces. These findings provide the first evidence for a specific and causal link between activity in category-selective networks and scalp-recorded ERP to their preferred categories. This result also demonstrates that the face and body N1 reflects several nonoverlapping neural sources, rather than changes in face-selective mechanisms alone. Lastly, because early stimulation (60-100 ms) affected selectivity of a later ERP component (150-200 ms), the results could imply a feed-forward connection between occipital and temporal category-selective areas.     

Implicit Processing of the Eyes and Mouth: Evidence from Human Electrophysiology

The current study examined the time course of implicit processing of distinct facial features and the associate event-related potential (ERP) components. To this end, we used a masked priming paradigm to investigate implicit processing of the eyes and mouth in upright and inverted faces, using a prime duration of 33 ms. Two types of prime-target pairs were used: 1. congruent (e.g., open eyes only in both prime and target or open mouth only in both prime and target); 2. incongruent (e.g., open mouth only in prime and open eyes only in target or open eyes only in prime and open mouth only in target). The identity of the faces changed between prime and target. Participants pressed a button when the target face had the eyes open and another button when the target face had the mouth open. The behavioral results showed faster RTs for the eyes in upright faces than the eyes in inverted faces, the mouth in upright and inverted faces. Moreover they also revealed a congruent priming effect for the mouth in upright faces. The ERP findings showed a face orientation effect across all ERP components studied (P1, N1, N170, P2, N2, P3) starting at about 80 ms, and a congruency/priming effect on late components (P2, N2, P3), starting at about 150 ms. Crucially, the results showed that the orientation effect was driven by the eye region (N170, P2) and that the congruency effect started earlier (P2) for the eyes than for the mouth (N2). These findings mark the time course of the processing of internal facial features and provide further evidence that the eyes are automatically processed and that they are very salient facial features that strongly affect the amplitude, latency, and distribution of neural responses to faces.     

Developmental prosopagnosia: a window to content-specific face processing

Developmental prosopagnosia is characterized by severely impaired face recognition. Individuals with this disorder, which often runs in families, have no history of brain damage and intact early visual processing systems. Recent research has also demonstrated that many developmental prosopagnosics have normal or relatively good object recognition, indicating that their impairments are not the result of deficits to a unitary visual recognition mechanism. To investigate the nature of the impaired mechanisms, extensive testing was done on an individual with especially pure face processing deficits. The results ruled out all extant explanations of prosopagnosia except one that proposed that faces are recognized by a content-specific face processing mechanism. fMRI and MEG studies show that there are a variety of neural profiles in developmental prosopagnosia, which is consistent with behavioral studies demonstrating that it is a heterogeneous disorder.     

Transcranial Direct Current Stimulation of the Dorsolateral Prefrontal Cortex Modulates Repetition Suppression to Unfamiliar Faces: An ERP Study

Repeated visual processing of an unfamiliar face suppresses neural activity in face-specific areas of the occipito-temporal cortex. This "repetition suppression" (RS) is a primitive mechanism involved in learning of unfamiliar faces, which can be detected through amplitude reduction of the N170 event-related potential (ERP). The dorsolateral prefrontal cortex (DLPFC) exerts top-down influence on early visual processing. However, its contribution to N170 RS and learning of unfamiliar faces remains unclear. Transcranial direct current stimulation (tDCS) transiently increases or decreases cortical excitability, as a function of polarity. We hypothesized that DLPFC excitability modulation by tDCS would cause polarity-dependent modulations of N170 RS during encoding of unfamiliar faces. tDCS-induced N170 RS enhancement would improve long-term recognition reaction time (RT) and/or accuracy rates, whereas N170 RS impairment would compromise recognition ability. Participants underwent three tDCS conditions in random order at ∼72 hour intervals: right anodal/left cathodal, right cathodal/left anodal and sham. Immediately following tDCS conditions, an EEG was recorded during encoding of unfamiliar faces for assessment of P100 and N170 visual ERPs. The P3a component was analyzed to detect prefrontal function modulation. Recognition tasks were administered ∼72 hours following encoding. Results indicate the right anodal/left cathodal condition facilitated N170 RS and induced larger P3a amplitudes, leading to faster recognition RT. Conversely, the right cathodal/left anodal condition caused N170 amplitude and RTs to increase, and a delay in P3a latency. These data demonstrate that DLPFC excitability modulation can influence early visual encoding of unfamiliar faces, highlighting the importance of DLPFC in basic learning mechanisms.     

Electrical Stimulation over Bilateral Occipito-Temporal Regions Reduces N170 in the Right Hemisphere and the Composite Face Effect

Transcranial direct current stimulation (tDCS) is a non-invasive brain stimulation technique that can modulate cortical excitability. Although the clinical value of tDCS has been advocated, the potential of tDCS in cognitive rehabilitation of face processing deficits is less understood. Face processing has been associated with the occipito-temporal cortex (OT). The present study investigated whether face processing in healthy adults can be modulated by applying tDCS over the OT. Experiment 1 investigated whether tDCS can affect N170, a face-sensitive ERP component, with a face orientation judgment task. The N170 in the right hemisphere was reduced in active stimulation conditions compared with the sham stimulation condition for both upright faces and inverted faces. Experiment 2 further demonstrated that tDCS can modulate the composite face effect, a type of holistic processing that reflects the obligatory attention to all parts of a face. The composite face effect was reduced in active stimulation conditions compared with the sham stimulation condition. Additionally, the current polarity did not modulate the effect of tDCS in the two experiments. The present study demonstrates that N170 can be causally manipulated by stimulating the OT with weak currents. Furthermore, our study provides evidence that obligatory attention to all parts of a face can be affected by the commonly used tDCS parameter setting.     

Sex-Differences of Face Coding: Evidence from Larger Right Hemispheric M170 in Men and Dipole Source Modelling

The processing of faces relies on a specialized neural system comprising bilateral cortical structures with a dominance of the right hemisphere. However, due to inconsistencies of earlier findings as well as more recent results such functional lateralization has become a topic of discussion. In particular, studies employing behavioural tasks and electrophysiological methods indicate a dominance of the right hemisphere during face perception only in men whereas women exhibit symmetric and bilateral face processing. The aim of this study was to further investigate such sex differences in hemispheric processing of personally familiar and opposite-sex faces using whole-head magnetoencephalography (MEG). We found a right-lateralized M170-component in occipito-temporal sensor clusters in men as opposed to a bilateral response in women. Furthermore, the same pattern was obtained in performing dipole localization and determining dipole strength in the M170-timewindow. These results suggest asymmetric involvement of face-responsive neural structures in men and allow to ascribe this asymmetry to the fusiform gyrus. This specifies findings from previous investigations employing event-related potentials (ERP) and LORETA reconstruction methods yielding rather extended bilateral activations showing left asymmetry in women and right lateralization in men. We discuss our finding of an asymmetric fusiform activation pattern in men in terms of holistic face processing during face evaluation and sex differences with regard to visual strategies in general and interest for opposite faces in special. Taken together the pattern of hemispheric specialization observed here yields new insights into sex differences in face perception and entails further questions about interactions between biological sex, psychological gender and influences that might be stimulus-driven or task dependent.