Early electrophysiological responses to multiple face orientations correlate with individual discrimination performance in humans

Picture-plane inversion dramatically impairs face recognition. Behavioral and event-related potential (ERP) studies suggest that this effect takes place during perceptual encoding of the face stimulus. However, the relationship between early electrophysiological responses to upright and inverted faces and the behavioral face inversion effect remains unclear. To address this question, we recorded ERPs while presenting 10 subjects with face photographs at 12 different orientations around the clock (30 degrees steps) during an individual face matching task. Using the variability in the electrophysiological responses introduced by the multiple orientations of the target face, we found a correlation between the ERP signal at 130-170 ms on occipito-temporal channels, and the behavioral performance measured on the probe stimulus. Correlations between ERP signal and behavioral performance started about 10 ms earlier in the right hemisphere. Significant effects of orientation were observed already at the level of the visual P1 (peaking at 100 ms), but the ERP signal was not correlated with behavior until the face-sensitive N170 time window. Overall, these observations indicate that plane-inversion affects the perceptual encoding of faces as early as 130 ms in occipito-temporal regions, leading directly to an increase in error rates and RTs during individual face recognition.     

Inversion and contrast polarity reversal affect both encoding and recognition processes of unfamiliar faces: a repetition study using ERPs.

Using ERPs in a face recognition task, we investigated whether inversion and contrast reversal, which seem to disrupt different aspects of face configuration, differentially affected encoding and memory for faces. Upright, inverted, and negative (contrast-reversed) unknown faces were either immediately repeated (0-lag) or repeated after 1 intervening face (1-lag). The encoding condition (new) consisted of the first presentation of items correctly recognized in the two repeated conditions. 0-lag faces were recognized better and faster than 1-lag faces. Inverted and negative pictures elicited longer reaction times, lower hit rates, and higher false alarm rates than upright faces. ERP analyses revealed that negative and inverted faces affected both early (encoding) and late (recognition) stages of face processing. Early components (N170, VPP) were delayed and enhanced by both inversion and contrast reversal which also affected P1 and P2 components. Amplitudes were higher for inverted faces at frontal and parietal sites from 350 to 600 ms. Priming effects were seen at encoding stages, revealed by shorter latencies and smaller amplitudes of N170 for repeated stimuli, which did not differ depending on face type. Repeated faces yielded more positive amplitudes than new faces from 250 to 450 ms frontally and from 400 to 600 ms parietally. However, ERP differences revealed that the magnitude of this repetition effect was smaller for negative and inverted than upright faces at 0-lag but not at 1-lag condition. Thus, face encoding and recognition processes were affected by inversion and contrast-reversal differently.     

Effects of repetition learning on upright, inverted and contrast-reversed face processing using ERPs

The effects of short-term learning on memory for inverted, contrast-reversed and upright faces were investigated using event-related potentials (ERPs) in a target/nontarget discrimination task following a learning phase of the target. Subjects were equally accurate for all three face types although responding more slowly to inverted and negative faces compared to upright faces. Face type affected both early ERP components P1 and N170, and long-latency components at frontal and parietal sites, reflecting the difficulty of processing inverted faces. Different effects of face type were found for P1 and N170 latencies and amplitudes, suggesting face processing could start around 100-120 ms and is sensitive to facial configuration. Repetition effects were also found on both early and long-latency components. Reduced N170 latency and amplitude for repeated targets are likely due to perceptual priming. Repetition effects on the N250 were delayed for inverted and negative faces, suggesting delayed access to stored facial representations for these formats. Increased frontopolar positivity at 250-300 ms and parietal positivity from 300 to 500 ms reflected familiarity 'old-new' repetition effects that were of similar magnitude for all three face types, indexing the accurate recognition of all faces. Thus, while structural encoding was disrupted by inversion and contrast-reversal, the learning phase was sufficient to abolish the effects of these configural manipulations behaviourally; all three face types were equally well recognised and this was reflected as equally large parietal old-new effects.     

Parametric design and correlational analyses help integrating fMRI and electrophysiological data during face processing

Face perception is typically associated with activation in the inferior occipital, superior temporal (STG), and fusiform gyri (FG) and with an occipitotemporal electrophysiological component peaking around 170 ms on the scalp, the N170. However, the relationship between the N170 and the multiple face-sensitive activations observed in neuroimaging is unclear. It has been recently shown that the amplitude of the N170 component monotonically decreases as gaussian noise is added to a picture of a face [Jemel et al., 2003]. To help clarify the sources of the N170 without a priori assumptions regarding their number and locations, ERPs and fMRI were recorded in five subjects in the same experiment, in separate sessions. We used a parametric paradigm in which the amplitude of the N170 was modulated by varying the level of noise in a picture, and identified regions where the percent signal change in fMRI correlated with the ERP data. N170 signals were observed for pictures of both cars and faces but were stronger for faces. A monotonic decrease with added noise was observed for the N170 at right hemisphere sites but was less clear on the left and occipital central sites. Correlations between fMRI signal and N170 amplitudes for faces were highly significant (P < 0.001) in bilateral fusiform gyrus and superior temporal gyrus. For cars, the strongest correlations were observed in the parahippocampal region and in the STG (P < 0.005). Besides contributing to clarify the spatiotemporal course of face processing, this study illustrates how ERP information may be used synergistically in fMRI analyses. Parametric designs may be developed further to provide some timing information on fMRI activity and help identify the generators of ERP signals.     

Is the rapid adaptation paradigm too rapid? Implications for face and object processing

Rapid adaptation is an adaptation procedure in which adaptors and test stimuli are presented in rapid succession. The current study tested the validity of this method for early ERP components by investigating the specificity of the adaptation effect on the face-sensitive N170 ERP component across multiple test stimuli. Experiments 1 and 2 showed identical response patterns for house and upright face test stimuli using the same adaptor stimuli. The results were also identical to those reported in a previous study using inverted face test stimuli (Nemrodov and Itier, 2011). In Experiment 3 all possible adaptor-test combinations between upright face, house, chair and car stimuli were used and no interaction between adaptor and test category, expected in the case of test-specific adaptation, was found. These results demonstrate that the rapid adaptation paradigm does not produce category-specific adaptation effects around 170-200 ms following test stimulus onset, a necessary condition for the interpretation of adaptation results. These results suggest the rapid categorical adaptation paradigm does not work.     

Pain modulates early sensory brain responses to task-irrelevant emotional faces

Background

Pain can have a significant impact on an individual's life, as it has both cognitive and affective consequences. However, our understanding of how pain affects social cognition is limited. Previous studies have shown that pain, as an alarm stimulus, can disrupt cognitive processing when focal attention is required, but whether pain also affects task-irrelevant perceptual processing remains unclear.

Methods

We examined the effect of laboratory-induced pain on event-related potentials (ERPs) to neutral, sad and happy faces before, during and after a cold pressor pain. ERPs reflecting different stages of visual processing (P1, N170 and P2) were analysed.

Results

Pain decreased the P1 amplitude for happy faces and increased the N170 amplitude for happy and sad faces compared to the pre-pain phase. The effect of pain on N170 was also observed in the post-pain phase. The P2 component was not affected by pain.

Conclusions

Our results suggest that pain alters both featural (P1) and structural face-sensitive (N170) visual encoding of emotional faces, even when the faces are irrelevant to the task. While the effect of pain on initial feature encoding seemed to be disruptive and specific to happy faces, later processing stages showed long-lasting and increased activity for both sad and happy emotional faces.

Significance

The observed alterations in face perception due to pain may have consequences for real-life interactions, as fast and automatic encoding of facial emotions is important for social interactions.     

Early lateralization and orientation tuning for face, word, and object processing in the visual cortex

Event-related potential (ERP) studies of the human brain have shown that object categories can be reliably distinguished as early as 130-170 ms on the surface of occipito-temporal cortex, peaking at the level of the N170 component. Consistent with this finding, neuropsychological and neuroimaging studies suggest major functional distinctions within the human object recognition system, particularly in hemispheric advantage, between the processing of words (left), faces (right), and objects (bilateral). Given these observations, our aim was to (1) characterize the differential response properties of the N170 to pictures of faces, objects, and words across hemispheres; and (2) test whether an effect of inversion for highly familiar and monooriented nonface stimuli such as printed words can be observed at the level of the N170. Scalp EEG (53 channels) was recorded in 15 subjects performing an orientation decision task with pictures of faces, words, and cars presented upright or inverted. All three categories elicited at the same latency a robust N170 component associated with a positive counterpart at centro-frontal sites (vertex-positive potential, VPP). While there were minor amplitude differences at the level of the occipital medial P1 between linguistic and nonlinguistic categories, scalp topographies and source analyses indicated strong hemispheric and orientation effects starting at the level of the N170, which was right lateralized for faces, smaller and bilateral for cars, and as large for printed words in the left hemisphere as for faces. The entire N170/VPP complex was accounted for by two dipolar sources located in the lateral inferior occipital cortex/posterior fusiform gyrus. These two locations were roughly equivalent across conditions but differed in strength and lateralization. Inversion delayed the N170 (and VPP) response for all categories, with an increasing delay for cars, words, and faces, respectively, as suggested by source modeling analysis. Such results show that early processes in object recognition respond to category-specific visual information, and are associated with strong lateralization and orientation bias.     

Face,eye and object early processing: What is the face specificity?

We investigated the human face specificity by comparing the effects of inversion and contrast reversal, two manipulations known to disrupt configural face processing, on human and ape faces, isolated eyes and objects, using event-related potentials. The face sensitive marker, N170, was shortest to human faces and delayed by inversion and contrast reversal for all categories and not only for human faces. Most importantly, N170 to inverted or contrast-reversed faces was not different from N170 to eyes that did not differ across manipulations. This suggests the disruption of facial configuration by these manipulations isolates the eye region from the face context, to which eye neurons respond. Our data suggest that (i) the inversion and contrast reversal effects on N170 latency are not specific to human faces and (ii) the similar increase of N170 amplitude by inversion and contrast reversal is unique to human faces and is driven by the eye region. Thus, while inversion and contrast reversal effects on N170 latency are not category-specific, their effects on amplitude are face-specific and reflect mainly the contribution of the eye region.     

Comparing neural correlates of configural processing in faces and objects: an ERP study of the Thatcher illusion

In the Thatcher illusion, a face with inverted eyes and mouth looks abnormal when upright but not when inverted. Behavioral studies have shown that thatcherization of an upright face disrupts perceptual processing of the local configuration. We recorded high-density EEG from normal observers to study ERP correlates of the illusion during the perception of faces and nonface objects, to determine whether inversion and thatcherization affect similar neural mechanisms. Observers viewed faces and houses in four conditions (upright vs. inverted, and normal vs. thatcherized) while detecting an oddball category (chairs). Thatcherization delayed the N170 component over occipito-temporal cortex to faces, but not to houses. This modulation matched the illusion as it was larger for upright than inverted faces. The P1 over medial occipital regions was delayed by face inversion but unaffected by thatcherization. Finally, face thatcherization delayed P2 over occipito-temporal but not over parietal regions, while inversion affected P2 across categories. All effects involving thatcherization were face-specific. These results indicate that effects of face inversion and feature inversion (in thatcherized faces) can be distinguished on a functional as well as neural level, and that they affect configural processing of faces in different time windows.     

Three stages of facial expression processing: ERP study with rapid serial visual presentation

Electrophysiological correlates of the processing facial expressions were investigated in subjects performing the rapid serial visual presentation (RSVP) task. The peak latencies of the event-related potential (ERP) components P1, vertex positive potential (VPP), and N170 were 165, 240, and 240 ms, respectively. The early anterior N100 and posterior P1 amplitudes elicited by fearful faces were larger than those elicited by happy or neutral faces, a finding which is consistent with the presence of a ‘negativity bias.’ The amplitude of the anterior VPP was larger when subjects were processing fearful and happy faces than when they were processing neutral faces; it was similar in response to fearful and happy faces. The late N300 and P300 not only distinguished emotional faces from neutral faces but also differentiated between fearful and happy expressions in lag2. The amplitudes of the N100, VPP, N170, N300, and P300 components and the latency of the P1 component were modulated by attentional resources. Deficient attentional resources resulted in decreased amplitude and increased latency of ERP components. In light of these results, we present a hypothetical model involving three stages of facial expression processing.     

Electrophysiological neural mechanisms for detection, configural analysis and recognition of faces

Despite ample explorations the nature of neural mechanisms underlying human expertise in face perception is still undetermined. Here we examined the response of two electrophysiological signals, the N170 ERP and induced gamma-band activity (>20 Hz), to face orientation and familiarity across two blocks, one in which the face identity was task-relevant and one in which it was not. N170 amplitude to inverted faces was higher than to upright faces and was not influenced by face familiarity or its task relevancy. In contrast, induced gamma activity was higher for upright than for inverted faces and for familiar than unfamiliar faces. The effect of face inversion was found in lower gamma frequency band (25-50 Hz), whereas familiarity affected amplitudes in higher gamma frequency band (50-70 Hz). For gamma, the relevance of face identity to the task modulated both inversion and familiarity effects. These findings pinpoint three functionally dissociated neural mechanisms involved in face processing, namely, detection, configural analysis, and recognition.     

An event-related potential component sensitive to images of the human body

One of the critical functions of vision is to provide information about other individuals. Neuroimaging experiments examining the cortical regions that analyze the appearance of other people have found partially overlapping networks that respond selectively to human faces and bodies. In event-related potential (ERP) studies, faces systematically elicit a negative component peaking 170 ms after presentation - the N170. To characterize the electrophysiological response to human bodies, we compared the ERPs elicited by faces, bodies and various control stimuli. In Experiment 1, a comparison of ERPs elicited by faces, bodies, objects and places showed that pictures of the human body (without the head) elicit a negative component peaking at 190 ms (an N190). While broadly similar to the N170, the N190 differs in both spatial distribution and amplitude from the N1 components elicited by faces, objects and scenes and peaks significantly later than the N170. The difference between N190 and N170 was further supported using topographic analyses of ERPs and source localization techniques. A unique, stable map topography was found to characterize human bodies between 130 and 230 ms. In Experiment 2, we tested the four conditions from Experiment 1, as well as intact and scrambled silhouettes and stick figures of the human body. We found that intact silhouettes and stick figures elicited significantly greater N190 amplitudes than their scrambled counterparts. Thus, the N190 generalizes to some degree to schematic depictions of the human form. Overall, our findings are consistent with intertwined, but functionally distinct, neural representations of the human face and body.     

Human face preference in gamma-frequency EEG activity

Previous studies demonstrated that induced EEG activity in the gamma band (iGBA) plays an important role in object recognition and is modulated by stimulus familiarity and its compatibility with pre-existent representations. In the present study we investigated the modulation of iGBA by the degree of familiarity and perceptual expertise that observers have with stimuli from different categories. Specifically, we compared iGBA in response to human faces versus stimuli which subjects are not expert with (ape faces, human hands, buildings and watches). iGBA elicited by human faces was higher and peaked earlier than that elicited by all other categories, which did not differ significantly from each other. These findings can be accounted for by two characteristics of perceptual expertise. One is the activation of a richer, stronger and, therefore, more easily accessible mental representation of human faces. The second is the more detailed perceptual processing necessary for within-category distinctions, which is the hallmark of perceptual expertise. In addition, the sensitivity of iGBA to human but not ape faces was contrasted with the face-sensitive N170-effect, which was similar for human and ape faces. In concert with previous studies, this dissociation suggests a multi-level neuronal model of face recognition, manifested by these two electrophysiological measures, discussed in this paper.     

Recognizing an individual face: 3D shape contributes earlier than 2D surface reflectance information

The human brain recognizes faces by means of two main diagnostic sources of information: three-dimensional (3D) shape and two-dimensional (2D) surface reflectance. Here we used event-related potentials (ERPs) in a face adaptation paradigm to examine the time-course of processing for these two types of information. With a 3D morphable model, we generated pairs of faces that were either identical, varied in 3D shape only, in 2D surface reflectance only, or in both. Sixteen human observers discriminated individual faces in these 4 types of pairs, in which a first (adapting) face was followed shortly by a second (test) face. Behaviorally, observers were as accurate and as fast for discriminating individual faces based on either 3D shape or 2D surface reflectance alone, but were faster when both sources of information were present. As early as the face-sensitive N170 component ( 160 ms following the test face), there was larger amplitude for changes in 3D shape relative to the repetition of the same face, especially over the right occipito-temporal electrodes. However, changes in 2D reflectance between the adapter and target face did not increase the N170 amplitude. At about 250 ms, both 3D shape and 2D reflectance contributed equally, and the largest difference in amplitude compared to the repetition of the same face was found when both 3D shape and 2D reflectance were combined, in line with observers' behavior. These observations indicate that evidence to recognize individual faces accumulate faster in the right hemisphere human visual cortex from diagnostic 3D shape information than from 2D surface reflectance information.     

Processing of famous faces and medial temporal lobe event-related potentials: a depth electrode study

The present study aims at analyzing the modulation of two types of event-related potentials originating from the human medial temporal lobe, the rhinal AMTL-N400 and the hippocampal P600 by the processing of famous faces. Therefore, we used a face recognition paradigm in which subjects had to discriminate the faces of famous persons from the faces of non-famous persons. Eleven patients with unilateral medial temporal lobe epilepsy undergoing intrahippocampal depth electrode recording for presurgical evaluation participated in this study. Event-related potentials (ERP) were recorded while a sequence of famous and non-famous faces was presented to the patients. The presentation of each face was repeated. The faces evoked N400-like potentials (anterior medial temporal lobe N400, AMTL-N400) in the rhinal cortex and P600-like potentials in the hippocampus. ERPs elicited by famous faces were contrasted with ERPs elicited by non-famous faces. The first presentation of famous faces elicited an enhanced AMTL-N400 and an enhanced hippocampal P600 in comparison to the second presentations of the famous faces or the (first and second presentation of the) non-famous faces. This findings are discussed in terms of associative semantic memory processes and the retrieval of person-specific information from long-term memory stores triggered by the processing of famous faces.     

Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170

A recent event-related potential (ERP) study (Thierry G., Martin, C.D., Downing, P., Pegna, A.J. 2007. Controlling for interstimulus perceptual variance abolishes N170 face selectivity. Nature Neuroscience, 10, 505-11) claimed that the larger occipito-temporal N170 response to pictures of faces than other categories -- the N170 effect -- is due to a methodological artifact in stimulus selection, specifically, a greater interstimulus physical variance between pictures of objects than faces in previous ERP studies which, when controlled, eliminates this N170 effect. This statement casts doubts on the validity of the conclusions reached by a whole tradition of electrophysiological experiments published over the past 15 years and questions the very interest of using the N170 to probe the time course of face processes in the human brain. Here we claim that this physical variance factor is ill-defined by Thierry et al. and cannot account for previous observations of a smaller N170 amplitude to nonface objects than faces without latency increase and component "smearing". Most importantly, this factor was controlled in previous studies that reported robust N170 effects. We demonstrate that the absence of N170 effect in the study of Thierry et al. is due to methodological flaws in the reported experiments, most notably measuring the N170 at the wrong electrode sites. Moreover, the authors attributed a modulation of N170 amplitude in their study to a differential interstimulus physical variance while it probably reflects a biased comparison of different quality sets of individual images. Here, by taking Thierry et al.'s study as an exemplar case of what should not be done in ERP research of visual categorization processes, we provide clarifications on a number of methodological and theoretical issues about the N170 and its largest amplitude to faces. More generally, we discuss the potential role of differential visual homogeneity of object categories as well as low-level visual properties versus high-level visual processes in accounting for early face-preferential responses and the question of the speed at which visual stimuli are categorized as faces. This survey of the literature points to the N170 as a critical event in the time course of face processes in the human brain.     

Species-specific response to human infant faces in the premotor cortex

The human infant face represents an essential source of communicative signals on the basis of which adults modulate their interactions with infants. Behavioral studies demonstrate that infants' faces activate sensitive and attuned responses in adults through their gaze, face expression, voice, and gesture. In this study we aimed to identify brain responses that underlie adults' general propensity to respond to infant faces. We recorded fMRI during adults' (non-parents) processing of unfamiliar infant faces compared to carefully matched adult faces and infrahuman mammal infant and adult faces. Human infant faces activated several brain systems including the lateral premotor cortex, supplementary motor area, cingulate cortex, anterior insula and the thalamus. Activation of these brain circuits suggests adults' preparation for communicative behavior with infants as well as attachment and caregiving. The same brain regions preferentially responded to human infant faces when compared to animal infant faces, indicating species-specific adult brain responses. Moreover, results of support vector machine based classification analysis indicated that these regions allowed above chance-level prediction of brain state during perception of human infant faces. The complex of brain responses to human infant faces appears to include biological mechanisms that underlie responsiveness and a caring inclination toward young children which appear to transcend adult's biological relationship to the baby.     

The N170, not the P1, indexes the earliest time for categorical perception of faces, regardless of interstimulus variance

A negative event-related potential (ERP) at occipito-temporal sites peaking around 150-170 ms after stimulus onset (N170) is typically larger for faces than other object categories. Most theories interpret this finding as due to face-selective processing in occipito-temporal and temporal cortex. However, a controversial account recently attributed the N170 effect to differences in interstimulus variance (ISV) among the images typically used for face and object conditions and proposed that the earlier P1 instead indexes the categorical processes generally attributed to the N170. This ERP study aimed to test this account definitively by using conditions in which the same face and object were shown repeatedly, eliminating both physical and perceptual ISV. Fourier amplitude spectra of faces and objects were matched to equate basic low-level visual properties that may affect early ERPs such as the P1. Results demonstrate that i) face selectivity of the N170 is largely preserved across many object categories after abolishing ISV, and ii) stimulus category does not modulate the P1. This conclusively refutes the ISV account while strongly supporting category as a critical factor driving N170 face selectivity.     

视觉完形负波在评价托吡酯及丙戊酸钠对癫痫患者早期认知功能损害中的应用

目的评价不完整面孔视觉加工中事件相关电位的特征及其在评价托吡酯及丙戊酸钠对癫痫患者认知损害的应用价值。方法30例未经治疗的癫痫患者分为两组：托吡酯治疗组及丙戊酸钠治疗组(各15例);另选择15名健康志愿者作为对照组。刺激物采用成对陌生且表情中性的灰阶面孔照片,刺激序列分2个状态：①完整状态(状态1)：S1和S2为相同或不同面孔相片;①不完整状态(状态2)：S1和S2为相同或不同面孔相片,且S2部分遮盖。S1和S2依次呈现,受试者任务：决定S2与S1是否为相同面孔相片,而忽略S2是否部分被遮盖,同步记录事件相关电位。结果3组受试者在面孔不完整状态下,均诱发出P100(P1)和N170(N1)。与完整面孔相比,不完整面孔在枕颞区诱发出明显增大的面孔负波N1,并且存在着右侧优势。在不完整面孔状态下,托吡酯组用药后N1波幅低于用药前(P<0.05);丙戊酸钠组在用药前、后N1峰波幅没有差别(P>0.05)。结论不完整面孔在枕颞区诱发出明显增大的面孔负波N170(N1);托吡酯对癫痫患者N1的损害较丙戊酸钠明显。     

Neural activation to upright and inverted faces in infants measured by near infrared spectroscopy

The present study examined infants' brain activity in response to upright and inverted faces using near infrared spectroscopy (NIRS), which can non-invasively record hemodynamic changes of the brain. NIRS is particularly useful for recording in infants, since recordings can be made, even while the infants are awake, without fixing their body and brain. For this objective, we used newly developed sensor probes of NIRS for recording in infants. We measured changes in cerebral oxygenation in 10 5-8-month-olds' left and right lateral areas while they were looking at upright and inverted faces. The results are summarized as follows: (1) the concentration of oxyhemoglobin (oxy-Hb) and total hemoglobin (total-Hb) increased significantly in the right lateral area during the upright face condition, (2) the concentration of total-Hb in the right lateral area differed significantly between the upright and inverted conditions, (3) hemodynamic changes were maximal in the temporal region, probably in the superior temporal sulcus (STS) in both hemispheres, and (4) the right hemisphere seems to be more important for recognizing upright faces. This is the first evidence showing that there is an inter-hemispheric difference on the effect of face inversion in the infant brain using a hemodynamic method.