EEG Frequency Tagging Reveals the Integration of Form and Motion Cues into the Perception of Group Movement.

The human brain has dedicated mechanisms for processing other people's movements. Previous research has revealed how these mechanisms contribute to perceiving the movements of individuals but has left open how we perceive groups of people moving together. Across three experiments, we test whether movement perception depends on the spatiotemporal relationships among the movements of multiple agents. In Experiment 1, we combine EEG frequency tagging with apparent human motion and show that posture and movement perception can be dissociated at harmonically related frequencies of stimulus presentation. We then show that movement but not posture processing is enhanced when observing multiple agents move in synchrony. Movement processing was strongest for fluently moving synchronous groups (Experiment 2) and was perturbed by inversion (Experiment 3). Our findings suggest that processing group movement relies on binding body postures into movements and individual movements into groups. Enhanced perceptual processing of movement synchrony may form the basis for higher order social phenomena such as group alignment and its social consequences.

The impact of stimulus size and orientation on individual face coding in monkey face-selective cortex.

Face-selective neurons in the monkey temporal cortex discharge at different rates in response to pictures of different individual faces. Here we tested whether this pattern of response across single neurons in the face-selective area ML (located in the middle Superior Temporal Sulcus) tolerates two affine transformations; picture-plane inversion, known to decrease the average response of face-selective neurons and the other, stimulus size. We recorded the response of 57 ML neurons in two awake and fixating monkeys. Face stimuli were presented at two sizes (10 and 5 degrees of visual angle) and two orientations (upright and inverted). Different faces elicited distinct patterns of activity across ML neurons that were reliable (i.e., predictable with a classifier) within a specific size and orientation condition. Despite observing a reduction in the average response magnitude of face-selective neurons to inverted faces, compared to upright faces, classifier performance was above chance for both upright and inverted faces. While decoding was largely preserved across changes in stimulus size, a classifier trained with one orientation condition and tested on the other did not lead to performance above chance level. We conclude that different individual faces can be decoded from patterns of responses in the monkey area ML regardless of orientation or size, but with qualitatively different patterns of responses for upright and inverted faces.

Gaze-Contingent Display Changes as New Window on Analytical and Holistic Face Perception in Children With Autism Spectrum Disorder.

The strength of holistic face perception in children with autism spectrum disorder (ASD) was evaluated by applying the gaze-contingent mask and window technique to a face matching and discrimination task in 6- to 14-year-old children with (n = 36) and without ASD (n = 47), and by examining fixation patterns. Behavioral results suggested a slower and less efficient face processing in the ASD sample compared with the matched control group. Comparing the moving mask and window conditions revealed a reduced holistic face processing bias in the younger age group but not in the older sample. Preferential viewing patterns revealed both similarities and differences between both participant groups.

Real-life experience with personally familiar faces enhances discrimination based on global information.

Despite the agreement that experience with faces leads to more efficient processing, the underlying mechanisms remain largely unknown. Building on empirical evidence from unfamiliar face processing in healthy populations and neuropsychological patients, the present experiment tested the hypothesis that personal familiarity is associated with superior discrimination when identity information is derived based on global, as opposed to local facial information. Diagnosticity and availability of local and global information was manipulated through varied physical similarity and spatial resolution of morph faces created from personally familiar or unfamiliar faces. We found that discrimination of subtle changes between highly similar morph faces was unaffected by familiarity. Contrariwise, relatively more pronounced physical (i.e., identity) differences were more efficiently discriminated for personally familiar faces, indicating more efficient processing of global, as opposed to local facial information through real-life experience.

The impact of orientation filtering on face-selective neurons in monkey inferior temporal cortex.

Faces convey complex social signals to primates. These signals are tolerant of some image transformations (e.g. changes in size) but not others (e.g. picture-plane rotation). By filtering face stimuli for orientation content, studies of human behavior and brain responses have shown that face processing is tuned to selective orientation ranges. In the present study, for the first time, we recorded the responses of face-selective neurons in monkey inferior temporal (IT) cortex to intact and scrambled faces that were filtered to selectively preserve horizontal or vertical information. Guided by functional maps, we recorded neurons in the lateral middle patch (ML), the lateral anterior patch (AL), and an additional region located outside of the functionally defined face-patches (CONTROL). We found that neurons in ML preferred horizontal-passed faces over their vertical-passed counterparts. Neurons in AL, however, had a preference for vertical-passed faces, while neurons in CONTROL had no systematic preference. Importantly, orientation filtering did not modulate the firing rate of neurons to phase-scrambled face stimuli in any recording region. Together these results suggest that face-selective neurons found in the face-selective patches are differentially tuned to orientation content, with horizontal tuning in area ML and vertical tuning in area AL.

Frequency tagging yields an objective neural signature of Gestalt formation.

The human visual system integrates separate visual inputs into coherently organized percepts, going beyond the information given. A striking example is the perception of an illusory square when physically separated inducers are positioned and oriented in a square-like configuration (illusory condition). This illusory square disappears when the specific configuration is broken, for instance, by rotating each inducer (non-illusory condition). Here we used frequency tagging and electroencephalography (EEG) to identify an objective neural signature of the global integration required for illusory surface perception. Two diagonal inducers were contrast-modulated at different frequency rates f1 and f2, leading to EEG responses exactly at these frequencies over the occipital cortex. Most importantly, nonlinear intermodulation (IM) components (e.g., f1+f2) appeared in the frequency spectrum, and were much larger in response to the illusory square figure than the non-illusory control condition. Since the IMs reflect long-range interactions between the signals from the inducers, these data provide an objective (i.e., at a precise and predicted EEG frequency) signature of neural processes involved in the emergence of illusory surface perception. More generally, these findings help to establish EEG frequency-tagging as a highly valuable approach to investigate the underlying neural mechanisms of subjective Gestalt phenomena in an objective and quantitative manner, at the system level in humans.

Neural Correlate of the Thatcher Face Illusion in a Monkey Face-Selective Patch.

Compelling evidence that our sensitivity to facial structure is conserved across the primate order comes from studies of the "Thatcher face illusion": humans and monkeys notice changes in the orientation of facial features (e.g., the eyes) only when faces are upright, not when faces are upside down. Although it is presumed that face perception in primates depends on face-selective neurons in the inferior temporal (IT) cortex, it is not known whether these neurons respond differentially to upright faces with inverted features. Using microelectrodes guided by functional MRI mapping, we recorded cell responses in three regions of monkey IT cortex. We report an interaction in the middle lateral face patch (ML) between the global orientation of a face and the local orientation of its eyes, a response profile consistent with the perception of the Thatcher illusion. This increased sensitivity to eye orientation in upright faces resisted changes in screen location and was not found among face-selective neurons in other areas of IT cortex, including neurons in another face-selective region, the anterior lateral face patch. We conclude that the Thatcher face illusion is correlated with a pattern of activity in the ML that encodes faces according to a flexible holistic template.

Face inversion and acquired prosopagnosia reduce the size of the perceptual field of view.

Using a gaze-contingent morphing approach, we asked human observers to choose one of two faces that best matched the identity of a target face: one face corresponded to the reference face's fixated part only (e.g., one eye), the other corresponded to the unfixated area of the reference face. The face corresponding to the fixated part was selected significantly more frequently in the inverted than in the upright orientation. This observation provides evidence that face inversion reduces an observer's perceptual field of view, even when both upright and inverted faces are displayed at full view and there is no performance difference between these conditions. It rules out an account of the drop of performance for inverted faces--one of the most robust effects in experimental psychology--in terms of a mere difference in local processing efficiency. A brain-damaged patient with pure prosopagnosia, viewing only upright faces, systematically selected the face corresponding to the fixated part, as if her perceptual field was reduced relative to normal observers. Altogether, these observations indicate that the absence of visual knowledge reduces the perceptual field of view, supporting an indirect view of visual perception.

A robust index of lexical representation in the left occipito-temporal cortex as evidenced by EEG responses to fast periodic visual stimulation.

Despite decades of research on reading, including the relatively recent contributions of neuroimaging and electrophysiology, identifying selective representations of whole visual words (in contrast to pseudowords) in the human brain remains challenging, in particular without an explicit linguistic task. Here we measured discrimination responses to written words by means of electroencephalography (EEG) during fast periodic visual stimulation. Sequences of pseudofonts, nonwords, or pseudowords were presented through sinusoidal contrast modulation at a periodic 10 Hz frequency rate (F), in which words were interspersed at regular intervals of every fifth item (i.e., F/5, 2 Hz). Participants monitored a central cross color change and had no linguistic task to perform. Within only 3 min of stimulation, a robust discrimination response for words at 2 Hz (and its harmonics, i.e., 4 and 6 Hz) was observed in all conditions, located predominantly over the left occipito-temporal cortex. The magnitude of the response was largest for words embedded in pseudofonts, and larger in nonwords than in pseudowords, showing that list context effects classically reported in behavioral lexical decision tasks are due to visual discrimination rather than decisional processes. Remarkably, the oddball response was significant even for the critical words/pseudowords discrimination condition in every individual participant. A second experiment replicated this words/pseudowords discrimination, and showed that this effect is not accounted for by a higher bigram frequency of words than pseudowords. Without any explicit task, our results highlight the potential of an EEG fast periodic visual stimulation approach for understanding the representation of written language. Its development in the scientific community might be valuable to rapidly and objectively measure sensitivity to word processing in different human populations, including neuropsychological patients with dyslexia and other reading difficulties.

The effect of face inversion for neurons inside and outside fMRI-defined face-selective cortical regions.

It is widely believed that face processing in the primate brain occurs in a network of category-selective cortical regions. Combined functional MRI (fMRI)-single-cell recording studies in macaques have identified high concentrations of neurons that respond more to faces than objects within face-selective patches. However, cells with a preference for faces over objects are also found scattered throughout inferior temporal (IT) cortex, raising the question whether face-selective cells inside and outside of the face patches differ functionally. Here, we compare the properties of face-selective cells inside and outside of face-selective patches in the IT cortex by means of an image manipulation that reliably disrupts behavior toward face processing: inversion. We recorded IT neurons from two fMRI-defined face-patches (ML and AL) and a region outside of the face patches (herein labeled OUT) during upright and inverted face stimulation. Overall, turning faces upside down reduced the firing rate of face-selective cells. However, there were differences among the recording regions. First, the reduced neuronal response for inverted faces was independent of stimulus position, relative to fixation, in the face-selective patches (ML and AL) only. Additionally, the effect of inversion for face-selective cells in ML, but not those in AL or OUT, was impervious to whether the neurons were initially searched for using upright or inverted stimuli. Collectively, these results show that face-selective cells differ in their functional characteristics depending on their anatomicofunctional location, suggesting that upright faces are preferably coded by face-selective cells inside but not outside of the fMRI-defined face-selective regions of the posterior IT cortex.

Face-specific impairment in holistic perception following focal lesion of the right anterior temporal lobe.

Recent studies have provided solid evidence for pure cases of prosopagnosia following brain damage. The patients reported so far have posterior lesions encompassing either or both the right inferior occipital cortex and fusiform gyrus, and exhibit a critical impairment in generating a sufficiently detailed holistic percept to individualize faces. Here, we extended these observations to include the prosopagnosic patient LR (Bukach, Bub, Gauthier, & Tarr, 2006), whose damage is restricted to the anterior region of the right temporal lobe. First, we report that LR is able to discriminate parametrically defined individual exemplars of nonface object categories as accurately and quickly as typical observers, which suggests that the visual similarity account of prosopagnosia does not explain his impairments. Then, we show that LR does not present with the typical face inversion effect, whole-part advantage, or composite face effect and, therefore, has impaired holistic perception of individual faces. Moreover, the patient is more impaired at matching faces when the facial part he fixates is masked than when it is selectively revealed by means of gaze contingency. Altogether these observations support the view that the nature of the critical face impairment does not differ qualitatively across patients with acquired prosopagnosia, regardless of the localization of brain damage: all these patients appear to be impaired to some extent at what constitutes the heart of our visual expertise with faces, namely holistic perception at a sufficiently fine-grained level of resolution to discriminate exemplars of the face class efficiently. This conclusion raises issues regarding the existing criteria for diagnosis/classification of patients as cases of apperceptive or associative prosopagnosia.

A steady-state visual evoked potential approach to individual face perception: effect of inversion, contrast-reversal and temporal dynamics.

Presentation of a face stimulus for several seconds at a periodic frequency rate leads to a right occipito-temporal evoked steady-state visual potential (SSVEP) confined to the stimulation frequency band. According to recent evidence (Rossion and Boremanse, 2011), this face-related SSVEP is largely reduced in amplitude when the exact same face is repeated at every stimulation cycle as compared to the presentation of different individual faces. Here this SSVEP individual face repetition effect was tested in 20 participants stimulated with faces at a 4 Hz rate for 84 s, in 4 conditions: faces upright or inverted, normal or contrast-reversed (2×2 design). To study the temporal dynamics of this effect, all stimulation sequences started with 15s of identical faces, after which, in half of the sequences, different faces were introduced. A larger response to different than identical faces at the fundamental (4 Hz) and second harmonic (8 Hz) components was observed for upright faces over the right occipito-temporal cortex. Weaker effects were found for inverted and contrast-reversed faces, two stimulus manipulations that are known to greatly affect the perception of facial identity. Addition of the two manipulations further decreased the effect. The phase of the fundamental frequency SSVEP response was delayed for inverted and contrast-reversed faces, to the same extent as the latency delay observed at the peak of the face-sensitive N170 component observed at stimulation sequence onset. Time-course analysis of the entire sequence of stimulation showed an immediate increase of 4Hz amplitude at the onset (16th second) of different face presentation, indicating a fast, large and frequency-specific release to individual face adaptation in the human brain. Altogether, these observations increase our understanding of the characteristics of the human steady-state face potential response and provide further support for the interest of this approach in the study of the neurofunctional mechanisms of face perception.

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, De Graef, Verfaillie, Busigny, & Rossion, 2010a; Van Belle, De Graef, Verfaillie, Rossion, & Lefèvre, 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.

Face inversion impairs holistic perception: evidence from gaze-contingent stimulation.

Human observers are experts at face recognition, yet a simple 180 degrees rotation of a face photograph decreases recognition performance substantially. A full understanding of this phenomenon-which is believed to be important for clarifying the nature of our expertise in face recognition-is still waiting. According to a long-standing and influential hypothesis, an inverted face cannot be perceived as holistically as an upright face and has to be analyzed local feature by local feature. Here, we tested this holistic perception hypothesis of the face inversion effect by means of a gaze-contingent stimulus presentation. When observers' perception was restricted to one fixated feature at a time by a gaze-contingent window, performance in an individual face matching task was almost unaffected by inversion. However, when a mask covered the fixated feature, preventing the use of local information at high resolution, the decrement of performance with inversion was even larger than in a normal-full view-condition. These observations provide evidence that the face inversion effect is caused by an inability to perceive the individual face as a whole rather than as a collection of specific features and thus support the view that observers' expertise at upright face recognition is due to the ability to perceive an individual face holistically.

Whole not hole: expert face recognition requires holistic perception.

Face recognition is an important ability of the human brain, yet its underlying mechanisms are still poorly understood. Two opposite views have been proposed to account for human face recognition expertise: the ability to extract the most diagnostic local information, feature-by feature (analytical view), or the ability to process all features at once over the whole face (holistic view). To help clarifying this debate, we used an original gaze-contingent stimulus presentation method to compare normal observers and a brain-damaged patient specifically impaired at face recognition (prosopagnosia). When a single central facial feature was revealed at a time through a gaze-contingent window, normal observers' performance at an individual face matching task decreased to the patient level. However, when only the central feature was masked, forcing normal observers to rely on the whole face but the fixated feature, their performance was almost not affected. In contrast, the prosopagnosic patient's performance decreased dramatically in this latter condition. These results were independent of the absolute size of the face and window/mask. This dissociation indicates that expertise in face recognition does not rest on the ability to analyze diagnostic local detailed features sequentially but rather on the ability to see the individual features of a face all at once, a function that is critically impaired in acquired prosopagnosia.

Fixation patterns during recognition of personally familiar and unfamiliar faces.

Previous studies recording eye gaze during face perception have rendered somewhat inconclusive findings with respect to fixation differences between familiar and unfamiliar faces. This can be attributed to a number of factors that differ across studies: the type and extent of familiarity with the faces presented, the definition of areas of interest subject to analyses, as well as a lack of consideration for the time course of scan patterns. Here we sought to address these issues by recording fixations in a recognition task with personally familiar and unfamiliar faces. After a first common fixation on a central superior location of the face in between features, suggesting initial holistic encoding, and a subsequent left eye bias, local features were focused and explored more for familiar than unfamiliar faces. Although the number of fixations did not differ for un-/familiar faces, the locations of fixations began to differ before familiarity decisions were provided. This suggests that in the context of familiarity decisions without time constraints, differences in processing familiar and unfamiliar faces arise relatively early - immediately upon initiation of the first fixation to identity-specific information - and that the local features of familiar faces are processed more than those of unfamiliar faces.

Configural and featural processing during face perception: a new stimulus set.

A new stimulus set of 60 male-face stimuli in seven in-depth orientations was developed. The set can be used in research on configural versus featural mechanisms of face processing. Configural, or holistic, changes are produced by changing the global form of the face, whereas featural, or part-based, changes are attained by altering the local form of internal facial features. For each face in the set, there is one other face that differs only by its global form and one other face that differs only by its internal features. In all faces, extrafacial cues have been eliminated or standardized. The stimulus set also contains a color-coded division of each face in areas of interest, which is useful for eye movement research on face scanning strategies. We report a matching experiment with upright and inverted face pairs that demonstrates that the face stimulus set is indeed useful for research on configural and featural face perception. The stimulus set may be downloaded from the Psychonomic Society's archive (brm.psychonomic-journals.org/content/supplemental) or from our Web site (http://ppw.kuleuven.be/labexppsy/newSite/resources).