Non-face Stimuli Research Articles

Individuals with Autistic-Like Traits Show Reduced Lateralization on a Greyscales Task

Individuals with autism spectrum conditions attend less to the left side of centrally presented face stimuli compared to neurotypical individuals, suggesting a reduction in right hemisphere activation. We examined whether a similar bias exists for non-facial stimuli in a large sample of neurotypical adults rated above- or below-average on the autism spectrum quotient (AQ). Using the "greyscales" task, we found the typical leftward bias in the below-average group was significantly reduced in the above-average group. Moreover, a negative correlation between leftward bias and the social skills factor of the AQ suggested a link between atypical hemispheric activation and social difficulties in high-AQ trait individuals that extends to non-facial stimuli.

Measuring the face-sensitive N170 with a gaming EEG system: A validation study

BackgroundThe N170 is a “face-sensitive” event-related potential (ERP) that occurs at around 170ms over occipito-temporal brain regions. The N170's potential to provide insight into the neural processing of faces in certain populations (e.g., children and adults with cognitive impairments) is limited by its measurement in scientific laboratories that can appear threatening to some people. New methodThe advent of cheap, easy-to-use portable gaming EEG systems provides an opportunity to record EEG in new contexts and populations. This study tested the validity of the face-sensitive N170 ERP measured with an adapted commercial EEG system (the Emotiv EPOC) that is used at home by gamers. ResultsThe N170 recorded through both the gaming EEG system and the research EEG system exhibited face-sensitivity, with larger mean amplitudes in response to the face stimuli than the non-face stimuli, and a delayed N170 peak in response to face inversion. Comparison with existing methodThe EPOC system produced very similar N170 ERPs to a research-grade Neuroscan system, and was capable of recording face-sensitivity in the N170, validating its use as research tool in this arena. ConclusionsThis opens new possibilities for measuring the face-sensitive N170 ERP in people who cannot travel to a traditional ERP laboratory (e.g., elderly people in care), who cannot tolerate laboratory conditions (e.g., people with autism), or who need to be tested in situ for practical or experimental reasons (e.g., children in schools)

Intelligent information loss: the coding of facial identity, head pose, and non-face information in the macaque face patch system.

Faces are a behaviorally important class of visual stimuli for primates. Recent work in macaque monkeys has identified six discrete face areas where most neurons have higher firing rates to images of faces compared with other objects (Tsao et al., 2006). While neurons in these areas appear to have different tuning (Freiwald and Tsao, 2010; Issa and DiCarlo, 2012), exactly what types of information and, consequently, which visual behaviors neural populations within each face area can support, is unknown. Here we use population decoding to better characterize three of these face patches (ML/MF, AL, and AM). We show that neural activity in all patches contains information that discriminates between the broad categories of face and nonface objects, individual faces, and nonface stimuli. Information is present in both high and lower firing rate regimes. However, there were significant differences between the patches, with the most anterior patch showing relatively weaker representation of nonface stimuli. Additionally, we find that pose-invariant face identity information increases as one moves to more anterior patches, while information about the orientation of the head decreases. Finally, we show that all the information we can extract from the population is present in patterns of activity across neurons, and there is relatively little information in the total activity of the population. These findings give new insight into the representations constructed by the face patch system and how they are successively transformed.

The role of the occipital face area in holistic processing involved in face detection and discrimination: A tDCS study.

The aim of this study was to examine the role of occipital face area (OFA) in mediating observers' tendency to perceive faces as "wholes" (holistic processing) both when detecting and discriminating faces. To investigate this issue, we modulated OFA activity using transcranial direct current stimulation (tDCS). In Experiment 1, participants performed a face detection task (the Mooney faces task) and a face discrimination task (the Composite faces task), which both assess holistic face processing. In Experiment 2, participants were asked to detect both Mooney faces and Mooney objects, to test face selectivity of OFA. In each experimental session, the tasks were presented once before (pre) and once after (post) administration of 20 min of excitability increasing anodal tDCS (real) and sham stimulation over the putative OFA. Compared with sham stimulation, we found that real anodal tDCS interfered with both Mooney faces and objects detection, whereas it had no effect on holistic processing involved in face discrimination, as measured by the Composite faces task. Our results suggest that OFA is causally implicated in facial detection at least in degraded conditions (i.e., when the "face" signal needs to be extracted from a noisy background). In turn, our data do not implicate OFA in holistic processing in face discrimination. Finally, our data suggest a possible role of OFA in categorization of other nonface stimuli, a conclusion that must be taken with caution, as stimulation over OFA may affect object-selective adjacent regions.

Startle eye-blink modulation by facial self-resemblance and current mood

Although salient stimuli are known to modulate startle eye-blink responses, and one's own face is considered of particular salience, effects of facial self-resemblance on startle responsiveness have not been systematically investigated. For the present study, pictures from the FACES database (rated as neutral) were digitally morphed to resemble the participants' (N=37) faces to varying degrees (25–50–75%). Perceptually matched geometrical shapes served as a control condition. At SOAs of either 300ms or 3000ms after picture onset, startle responses were elicited by white noise (50ms, 105dB), and recorded at the orbicularis oculi via EMG. Prior to the experiment, self-reported mood was assessed by means of the PANAS. Relative to non-face stimuli, the presentation of faces reduced startle magnitude at short, but not long, lead intervals. Furthermore, for probes presented at a SOA of 300ms, a linear decrease in startle magnitude with higher levels of self-resemblance was observed, presumably reflecting higher salience of the self-face. The startle modulating effect of self-resembling faces during longer lead intervals was moderated by the participants' current mood: negative affect predicted stronger patterns of attenuation, which might be interpreted as an increase in self-focus resulting from more negative mood.

Behavioral and neural correlates of facial versus nonfacial stimuli processing in adults with ADHD: An ERP study.

The present study was aimed at identifying behavioral and neural correlates of face processing in adults with attention-deficit/hyperactivity disorder (ADHD) using scalp-recorded event-related potentials (ERPs). Behavioral and ERP responses were examined using a 4-stimulus visual oddball task, combining facial and nonfacial stimuli. Responses to target and nontarget stimuli were compared across groups of young adults with ADHD and comparison subjects. Participants with ADHD had poorer performance than controls on all indices of the oddball task. Higher rates of omissions and slower reaction times (RTs) of ADHD participants compared with controls had been found only in response to face targets but not in response to nonfacial targets. ERP results indicated that ADHD significantly interacted with the type of target stimuli. Participants with ADHD, compared with controls, showed a pronounced reduction in P3 and N3 amplitudes in response to face targets but not in response to nonfacial targets. The current results provide indication of modulation of face processing in adults with ADHD. ERP alterations, reflected in abnormally reduced P3 and N3 to face targets, may suggest ADHD-related abnormal recruitment of neural resources to process face stimuli. Behavioral and brain function measures of face processing may provide valuable additional tools for use in clinical assessment of ADHD in adulthood.

The N170 observed 'in the wild': robust event-related potentials to faces in cluttered dynamic visual scenes.

As a social species in a constantly changing environment, humans rely heavily on the informational richness and communicative capacity of the face. Thus, understanding how the brain processes information about faces in real-time is of paramount importance. The N170 is a high-temporal resolution electrophysiological index of the brain's early response to visual stimuli that is reliably elicited in carefully controlled laboratory-based studies. Although the N170 has often been reported to be of greatest amplitude to faces, there has been debate regarding whether this effect might be an artefact of certain aspects of the controlled experimental stimulation schedules and materials. To investigate whether the N170 can be identified in more realistic conditions with highly variable and cluttered visual images and accompanying auditory stimuli we recorded EEG 'in the wild', while participants watched pop videos. Scene-cuts to faces generated a clear N170 response, and this was larger than the N170 to transitions where the videos cut to non-face stimuli. Within participants, wild-type face N170 amplitudes were moderately correlated to those observed in a typical laboratory experiment. Thus, we demonstrate that the face N170 is a robust and ecologically valid phenomenon and not an artefact arising as an unintended consequence of some property of the more typical laboratory paradigm.

Effect of familiarity on reward anticipation in children with and without autism spectrum disorders.

BackgroundPrevious research on the reward system in autism spectrum disorders (ASD) suggests that children with ASD anticipate and process social rewards differently than typically developing (TD) children—but has focused on the reward value of unfamiliar face stimuli. Children with ASD process faces differently than their TD peers. Previous research has focused on face processing of unfamiliar faces, but less is known about how children with ASD process familiar faces. The current study investigated how children with ASD anticipate rewards accompanied by familiar versus unfamiliar faces.MethodsThe stimulus preceding negativity (SPN) of the event-related potential (ERP) was utilized to measure reward anticipation. Participants were 6- to 10-year-olds with (N = 14) and without (N = 14) ASD. Children were presented with rewards accompanied by incidental face or non-face stimuli that were either familiar (caregivers) or unfamiliar. All non-face stimuli were composed of scrambled face elements in the shape of arrows, controlling for visual properties.ResultsNo significant differences between familiar versus unfamiliar faces were found for either group. When collapsing across familiarity, TD children showed larger reward anticipation to face versus non-face stimuli, whereas children with ASD did not show differential responses to these stimulus types. Magnitude of reward anticipation to faces was significantly correlated with behavioral measures of social impairment in the ASD group.ConclusionsThe findings do not provide evidence for differential reward anticipation for familiar versus unfamiliar face stimuli in children with or without ASD. These findings replicate previous work suggesting that TD children anticipate rewards accompanied by social stimuli more than rewards accompanied by non-social stimuli. The results do not support the idea that familiarity normalizes reward anticipation in children with ASD. Our findings also suggest that magnitude of reward anticipation to faces is correlated with levels of social impairment for children with ASD.

When does repetition suppression depend on repetition probability?

When does repetition suppression depend on repetition probability?

Repetition probability effects depend on prior experiences

The magnitude of repetition suppression (RS) in the Fusiform Face Area is influenced by the probability of repetitions of faces (Summerfield et al., 2008), implying that perceptual expectations affect repetition-related processes. Surprisingly, however, macaque single-cell (Kaliukhovich and Vogels, 2011) and human fMRI (Kovacs et al., 2013) studies have failed to find repetition probability [P(rep)] modulations of RS with nonface stimuli in the occipitotemporal cortex, suggesting that the effect is face specific. One possible explanation of this category selectivity is that the extensive experience humans have with faces affects the neural mechanisms of RS specifically, creating P(rep) modulatory effects. To address this question, we used fMRI to test the P(rep) effects for another well trained stimulus category, upright letters of the roman alphabet as well as for unfamiliar false fonts. We observed significant RS for both stimulus sets in the Letter Form Area as well as in the caudodorsal part of the lateral occipital complex. Interestingly, the influence of P(rep) on RS was dependent on the stimulus: while we observed P(rep) modulations for the roman letters, no such effects were found for the unfamiliar false fonts in either area. Our findings suggest that P(rep) effects on RS are manifest for nonface stimuli as well, but that they depend on the experience of the subjects with the stimulus category. This shows, for the first time, that prior experience affects the influence of contextual predictive information on RS in the human occipitotemporal cortex.

Developmental plateau in visual object processing from adolescence to adulthood in autism

A lack of typical age-related improvement from adolescence to adulthood contributes to face recognition deficits in adults with autism on the Cambridge Face Memory Test (CFMT). The current studies examine if this atypical developmental trajectory generalizes to other tasks and objects, including parts of the face. The CFMT tests recognition of whole faces, often with a substantial delay. The current studies used the immediate memory (IM) task and the parts-whole face task from the Let’s Face It! battery, which examines whole faces, face parts, and cars, without a delay between memorization and test trials. In the IM task, participants memorize a face or car. Immediately after the target disappears, participants identify the target from two similar distractors. In the part-whole task, participants memorize a whole face. Immediately after the face disappears, participants identify the target from a distractor with different eyes or mouth, either as a face part or a whole face.Results indicate that recognition deficits in autism become more robust by adulthood, consistent with previous work, and also become more general, including cars. In the IM task, deficits in autism were specific to faces in childhood, but included cars by adulthood. In the part-whole task, deficits in autism became more robust by adulthood, including both eyes and mouths as parts and in whole faces. Across tasks, the deficit in autism increased between adolescence and adulthood, reflecting a lack of typical improvement, leading to deficits with non-face stimuli and on a task without a memory delay. These results suggest that brain maturation continues to be affected into adulthood in autism, and that the transition from adolescence to adulthood is a vulnerable stage for those with autism.

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.

Holistic processing and reliance on global viewing strategies in older adults' face perception

There is increasing evidence that face recognition might be impaired in older adults, but it is unclear whether the impairment is truly perceptual, and face specific. In order to address this question we compared performance in same/different matching tasks with face and non-face objects (watches) among young (mean age 23.7) and older adults (mean age 70.4) using a context congruency paradigm (Meinhardt-Injac, Persike & Meinhardt, 2010, Meinhardt-Injac, Persike and Meinhardt, 2011a). Older adults were less accurate than young adults with both object classes, while face matching was notably impaired. Effects of context congruency and inversion, measured as the hallmarks of holistic processing, were equally strong in both age groups, and were found only for faces, but not for watches. The face specific decline in older adults revealed deficits in handling internal facial features, while young adults matched external and internal features equally well. Comparison with non-face stimuli showed that this decline was face specific, and did not concern processing of object features in general. Taken together, the results indicate no age-related decline in the capabilities to process faces holistically. Rather, strong holistic effects, combined with a loss of precision in handling internal features indicate that older adults rely on global viewing strategies for faces. At the same time, access to the exact properties of inner face details becomes restricted.

Novelty preference in face perception by week-old lambs (Ovis aries)

An extensive literature has been accumulating, in recent years, on face-processing in sheep and on the relevance of faces for social interaction in this species. In spite of this, spontaneous preferences for face or non-face stimuli in lambs have not been reported. In this study we tested the spontaneous preference of 8-day-old lambs (N = 9) for three pairs of stimuli. In each pair, one stimulus was a face-like display, whereas the other presented the same inner features displaced in unnatural positions. One pair of stimuli was obtained from photographic images of ewes’ faces, the other two pairs were schematic face-like stimuli. Lambs could differentiate the two stimuli obtained by photos of conspecifics, looking longer at the non-face stimulus (p < 0.05). We interpret this as a novelty preference, proving that few day-old lambs have already encoded the structural properties that define a face and recognize violations of those general properties.

Reward anticipation and processing of social versus nonsocial stimuli in children with and without autism spectrum disorders.

How children respond to social and nonsocial rewards has important implications for both typical and atypical social-cognitive development. Individuals with autism spectrum disorders (ASD) are thought to process rewards differently than typically developing (TD) individuals. However, there is little direct evidence to support this claim. Two event-related potentials were measured. The stimulus preceding negativity (SPN) was utilized to measure reward anticipation, and the feedback related negativity (FRN) was utilized to measure reward processing. Participants were 6- to 8-year-olds with (N=20) and without (N=23) ASD. Children were presented with rewards accompanied by incidental face or nonface stimuli. Nonface stimuli were composed of scrambled face elements in the shape of arrows, controlling for low-level visual properties. Children with ASD showed smaller responses while anticipating and processing rewards accompanied by social stimuli than TD children. Anticipation and processing of rewards accompanied by nonsocial stimuli was intact in children with ASD. This is the first study to measure both reward anticipation and processing in ASD while controlling for reward properties. The findings provide evidence that children with autism have reward anticipation and processing deficits for social stimuli only. Our results suggest that while typically developing children find social stimuli more salient than nonsocial stimuli, children with ASD may have the opposite preference.

Integration of internal and external facial features in 8- to 10-year-old children and adults

Investigation of whole-part and composite effects in 4- to 6-year-old children gave rise to claims that face perception is fully mature within the first decade of life (Crookes & McKone, 2009). However, only internal features were tested, and the role of external features was not addressed, although external features are highly relevant for holistic face perception (Sinha & Poggio, 1996; Axelrod & Yovel, 2010, 2011). In this study, 8- to 10-year-old children and adults performed a same–different matching task with faces and watches. In this task participants attended to either internal or external features. Holistic face perception was tested using a congruency paradigm, in which face and non-face stimuli either agreed or disagreed in both features (congruent contexts) or just in the attended ones (incongruent contexts). In both age groups, pronounced context congruency and inversion effects were found for faces, but not for watches. These findings indicate holistic feature integration for faces. While inversion effects were highly similar in both age groups, context congruency effects were stronger for children. Moreover, children's face matching performance was generally better when attending to external compared to internal features. Adults tended to perform better when attending to internal features. Our results indicate that both adults and 8- to 10-year-old children integrate external and internal facial features into holistic face representations. However, in children's face representations external features are much more relevant. These findings suggest that face perception is holistic but still not adult-like at the end of the first decade of life.

Repetition probability effects depend on prior experiences.

The magnitude of repetition suppression (RS) in the Fusiform Face Area is influenced by the probability of repetitions of faces (Summerfield et al., 2008), implying that perceptual expectations affect repetition-related processes. Surprisingly, however, macaque single-cell (Kaliukhovich and Vogels, 2011) and human fMRI (Kovács et al., 2013) studies have failed to find repetition probability [P(rep)] modulations of RS with nonface stimuli in the occipitotemporal cortex, suggesting that the effect is face specific. One possible explanation of this category selectivity is that the extensive experience humans have with faces affects the neural mechanisms of RS specifically, creating P(rep) modulatory effects. To address this question, we used fMRI to test the P(rep) effects for another well trained stimulus category, upright letters of the roman alphabet as well as for unfamiliar false fonts. We observed significant RS for both stimulus sets in the Letter Form Area as well as in the caudodorsal part of the lateral occipital complex. Interestingly, the influence of P(rep) on RS was dependent on the stimulus: while we observed P(rep) modulations for the roman letters, no such effects were found for the unfamiliar false fonts in either area. Our findings suggest that P(rep) effects on RS are manifest for nonface stimuli as well, but that they depend on the experience of the subjects with the stimulus category. This shows, for the first time, that prior experience affects the influence of contextual predictive information on RS in the human occipitotemporal cortex.

Phase noise reveals early category-specific modulation of the event-related potentials.

Previous studies have found that the amplitude of the early event-related potential (ERP) components evoked by faces, such as N170 and P2, changes systematically as a function of noise added to the stimuli. This change has been linked to an increased perceptual processing demand and to enhanced difficulty in perceptual decision making about faces. However, to date it has not yet been tested whether noise manipulation affects the neural correlates of decisions about face and non-face stimuli similarly. To this end, we measured the ERPs for faces and cars at three different phase noise levels. Subjects performed the same two-alternative age-discrimination task on stimuli chosen from young–old morphing continua that were created from faces as well as cars and were calibrated to lead to similar performances at each noise-level. Adding phase noise to the stimuli reduced performance and enhanced response latency for the two categories to the same extent. Parallel to that, phase noise reduced the amplitude and prolonged the latency of the face-specific N170 component. The amplitude of the P1 showed category-specific noise dependence: it was enhanced over the right hemisphere for cars and over the left hemisphere for faces as a result of adding phase noise to the stimuli, but remained stable across noise levels for cars over the left and for faces over the right hemisphere. Moreover, noise modulation altered the category-selectivity of the N170, while the P2 ERP component, typically associated with task decision difficulty, was larger for the more noisy stimuli regardless of stimulus category. Our results suggest that the category-specificity of noise-induced modulations of ERP responses starts at around 100 ms post-stimulus.

Rapid, high-frequency, and theta-coupled gamma oscillations in the inferior occipital gyrus during face processing

Neuroimaging studies have found greater activation in the inferior occipital gyrus (IOG), or occipital face area, in response to faces relative to non-facial stimuli. However, the temporal, frequency, and functional profiles of IOG activity during face processing remain unclear. Here, this issue was investigated by recording intracranial field potentials in the IOG during the presentation of faces, mosaics, and houses in upright and inverted orientations. Time–frequency statistical parametric mapping analyses revealed greater gamma-band activation in the IOG beginning at 110 msec and covering 40–300 Hz in response to upright faces relative to upright houses and mosaics. Phase–amplitude cross-frequency coupling analyses revealed more evident theta–gamma couplings at 115–256 msec during the processing of upright faces as compared with that of upright houses and mosaics. Comparable gamma-band activity was observed during the processing of inverted and upright faces at about 100–200 msec, but weaker activity and different coupling with theta-band activity after 200 msec. These patterns of activity were more evident in the right than in the left IOG. These results, together with other evidence on neural communication, suggest that broadband gamma oscillations in the right IOG conduct rapid and multistage (i.e., both featural and configural) face processing in collaboration with theta oscillations transmitted from other brain regions.

Local feature suppression effect in face and non-face stimuli

There is evidence that the cognitive system processes human faces faster and more precisely than other stimuli. Also, faces summon visual attention in an automatic manner, as evidenced by efficient, 'pop-out' search for face targets amongst homogeneous non-face distractors. Pop-out for faces implies that faces are processed as a basic visual 'feature' by specialized face-tuned detectors, similar to the coding of other features (e.g., color, orientation, motion, etc.). However, it is unclear whether such face detectors encode only the global face configuration or both global and local face features. If the former were correct, the face detectors should be unable to support search for a local face feature, rendering search slower relative to non-face stimuli; that is, there would be local feature suppression (LFS) for faces. If the latter was the case, there should be no difference in the processing of local and, respectively, global face features. In two experiments, participants discerned the presence (vs. absence) of a local target defined as a part of either a normal or a scrambled (schematic or realistic) face or of a non-face (Kanizsa diamond or realistic house) configuration. The results consistently showed a robust LFS effect in both reaction times and error rates for face stimuli, and either no difference or even a local feature enhancement effect for the control stimuli. Taken together, these findings indicate that faces are encoded as a basic visual feature by means of globally tuned face detectors.