Face inversion reduces the persistence of global form and its neural correlates

Face inversion produces a detrimental effect on face recognition. The extent to which the inversion of faces and other kinds of objects influences the perceptual binding of visual information into global forms is not known. We used a behavioral method and functional MRI (fMRI) to measure the effect of face inversion on visual persistence, a type of perceptual memory that reflects sustained awareness of global form. We found that upright faces persisted longer than inverted versions of the same images; we observed a similar effect of inversion on the persistence of animal stimuli. This effect of inversion on persistence was evident in sustained fMRI activity throughout the ventral visual hierarchy, including the lateral occipital area (LO), two face-selective visual areas--the fusiform face area (FFA) and the occipital face area (OFA)--and several early visual areas. V1 showed the same initial fMRI activation to upright and inverted forms but this activation lasted longer for upright stimuli. The inversion effect on persistence-related fMRI activity in V1 and other retinotopic visual areas demonstrates that higher-tier visual areas influence early visual processing via feedback. This feedback effect on figure-ground processing is sensitive to the orientation of the figure.     

Face perception: domain specific, not process specific

Evidence that face perception is mediated by special cognitive and neural mechanisms comes from fMRI studies of the fusiform face area (FFA) and behavioral studies of the face inversion effect. Here, we used these two methods to ask whether face perception mechanisms are stimulus specific, process specific, or both. Subjects discriminated pairs of upright or inverted faces or house stimuli that differed in either the spatial distance among parts (configuration) or the shape of the parts. The FFA showed a much higher response to faces than to houses, but no preference for the configuration task over the part task. Similarly, the behavioral inversion effect was as large in the part task as the configuration task for faces, but absent in both part and configuration tasks for houses. These findings indicate that face perception mechanisms are not process specific for parts or configuration but are domain specific for face stimuli per se.     

The neuropsychology of face perception: beyond simple dissociations and functional selectivity

Face processing relies on a distributed, patchy network of cortical regions in the temporal and frontal lobes that respond disproportionately to face stimuli, other cortical regions that are not even primarily visual (such as somatosensory cortex), and subcortical structures such as the amygdala. Higher-level face perception abilities, such as judging identity, emotion and trustworthiness, appear to rely on an intact face-processing network that includes the occipital face area (OFA), whereas lower-level face categorization abilities, such as discriminating faces from objects, can be achieved without OFA, perhaps via the direct connections to the fusiform face area (FFA) from several extrastriate cortical areas. Some lesion, transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) findings argue against a strict feed-forward hierarchical model of face perception, in which the OFA is the principal and common source of input for other visual and non-visual cortical regions involved in face perception, including the FFA, face-selective superior temporal sulcus and somatosensory cortex. Instead, these findings point to a more interactive model in which higher-level face perception abilities depend on the interplay between several functionally and anatomically distinct neural regions. Furthermore, the nature of these interactions may depend on the particular demands of the task. We review the lesion and TMS literature on this topic and highlight the dynamic and distributed nature of face processing.     

Orientation-contingent face aftereffects and implications for face-coding mechanisms

Humans have an impressive ability to discriminate between faces despite their similarity as visual patterns. This expertise relies on configural coding of spatial relations between face features and/or holistic coding of overall facial structure. These expert face-coding mechanisms appear to be engaged most effectively by upright faces, with inverted faces engaging primarily feature-coding mechanisms. We show that opposite figural aftereffects can be induced simultaneously for upright and inverted faces, demonstrating that distinct neural populations code upright and inverted faces. This result also suggests that expert (upright) face-coding mechanisms can be selectively adapted. These aftereffects occur for judgments of face normality and face gender and are robust to changes in face size, ruling out adaptation of low-level, retinotopically organized coding mechanisms. Our results suggest a resolution of a paradox in the face recognition literature. Neuroimaging studies have found surprisingly little orientation selectivity in the fusiform face area (FFA) despite evidence that this region plays a role in expert face coding and that expert face-coding mechanisms are selectively engaged by upright faces. Our results, demonstrating orientation-contingent adaptation of face-coding mechanisms, suggest that the FFA's apparent lack of orientation selectivity may be an artifact of averaging across distinct populations within the FFA that respond to upright and inverted faces.     

The fusiform face area is engaged in holistic, not parts-based, representation of faces

Numerous studies with functional magnetic resonance imaging have shown that the fusiform face area (FFA) in the human brain plays a key role in face perception. Recent studies have found that both the featural information of faces (e.g., eyes, nose, and mouth) and the configural information of faces (i.e., spatial relation among features) are encoded in the FFA. However, little is known about whether the featural information is encoded independent of or combined with the configural information in the FFA. Here we used multi-voxel pattern analysis to examine holistic representation of faces in the FFA by correlating spatial patterns of activation with behavioral performance in discriminating face parts with face configurations either present or absent. Behaviorally, the absence of face configurations (versus presence) impaired discrimination of face parts, suggesting a holistic representation in the brain. Neurally, spatial patterns of activation in the FFA were more similar among correct than incorrect trials only when face parts were presented in a veridical face configuration. In contrast, spatial patterns of activation in the occipital face area, as well as the object-selective lateral occipital complex, were more similar among correct than incorrect trials regardless of the presence of veridical face configurations. This finding suggests that in the FFA faces are represented not on the basis of individual parts but in terms of the whole that emerges from the parts.     

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.     

The Hierarchical Brain Network for Face Recognition

Numerous functional magnetic resonance imaging (fMRI) studies have identified multiple cortical regions that are involved in face processing in the human brain. However, few studies have characterized the face-processing network as a functioning whole. In this study, we used fMRI to identify face-selective regions in the entire brain and then explore the hierarchical structure of the face-processing network by analyzing functional connectivity among these regions. We identified twenty-five regions mainly in the occipital, temporal and frontal cortex that showed a reliable response selective to faces (versus objects) across participants and across scan sessions. Furthermore, these regions were clustered into three relatively independent sub-networks in a face-recognition task on the basis of the strength of functional connectivity among them. The functionality of the sub-networks likely corresponds to the recognition of individual identity, retrieval of semantic knowledge and representation of emotional information. Interestingly, when the task was switched to object recognition from face recognition, the functional connectivity between the inferior occipital gyrus and the rest of the face-selective regions were significantly reduced, suggesting that this region may serve as an entry node in the face-processing network. In sum, our study provides empirical evidence for cognitive and neural models of face recognition and helps elucidate the neural mechanisms underlying face recognition at the network level.     

Regional Neural Response Differences in the Determination of Faces or Houses Positioned in a Wide Visual Field

In human visual cortex, the primary visual cortex (V1) is considered to be essential for visual information processing; the fusiform face area (FFA) and parahippocampal place area (PPA) are considered as face-selective region and places-selective region, respectively. Recently, a functional magnetic resonance imaging (fMRI) study showed that the neural activity ratios between V1 and FFA were constant as eccentricities increasing in central visual field. However, in wide visual field, the neural activity relationships between V1 and FFA or V1 and PPA are still unclear. In this work, using fMRI and wide-view present system, we tried to address this issue by measuring neural activities in V1, FFA and PPA for the images of faces and houses aligning in 4 eccentricities and 4 meridians. Then, we further calculated ratio relative to V1 (RRV1) as comparing the neural responses amplitudes in FFA or PPA with those in V1. We found V1, FFA, and PPA showed significant different neural activities to faces and houses in 3 dimensions of eccentricity, meridian, and region. Most importantly, the RRV1s in FFA and PPA also exhibited significant differences in 3 dimensions. In the dimension of eccentricity, both FFA and PPA showed smaller RRV1s at central position than those at peripheral positions. In meridian dimension, both FFA and PPA showed larger RRV1s at upper vertical positions than those at lower vertical positions. In the dimension of region, FFA had larger RRV1s than PPA. We proposed that these differential RRV1s indicated FFA and PPA might have different processing strategies for encoding the wide field visual information from V1. These different processing strategies might depend on the retinal position at which faces or houses are typically observed in daily life. We posited a role of experience in shaping the information processing strategies in the ventral visual cortex.     

Explicating the Face Perception Network with White Matter Connectivity

A network of multiple brain regions is recruited in face perception. Our understanding of the functional properties of this network can be facilitated by explicating the structural white matter connections that exist between its functional nodes. We accomplished this using functional MRI (fMRI) in combination with fiber tractography on high angular resolution diffusion weighted imaging data. We identified the three nodes of the core face network: the “occipital face area” (OFA), the “fusiform face area” (mid-fusiform gyrus or mFus), and the superior temporal sulcus (STS). Additionally, a region of the anterior temporal lobe (aIT), implicated as being important for face perception was identified. Our data suggest that we can further divide the OFA into multiple anatomically distinct clusters – a partitioning consistent with several recent neuroimaging results. More generally, structural white matter connectivity within this network revealed: 1) Connectivity between aIT and mFus, and between aIT and occipital regions, consistent with studies implicating this posterior to anterior pathway as critical to normal face processing; 2) Strong connectivity between mFus and each of the occipital face-selective regions, suggesting that these three areas may subserve different functional roles; 3) Almost no connectivity between STS and mFus, or between STS and the other face-selective regions. Overall, our findings suggest a re-evaluation of the “core” face network with respect to what functional areas are or are not included in this network.     

Sensory competition in the face processing areas of the human brain

The concurrent presentation of multiple stimuli in the visual field may trigger mutually suppressive interactions throughout the ventral visual stream. While several studies have been performed on sensory competition effects among non-face stimuli relatively little is known about the interactions in the human brain for multiple face stimuli. In the present study we analyzed the neuronal basis of sensory competition in an event-related functional magnetic resonance imaging (fMRI) study using multiple face stimuli. We varied the ratio of faces and phase-noise images within a composite display with a constant number of peripheral stimuli, thereby manipulating the competitive interactions between faces. For contralaterally presented stimuli we observed strong competition effects in the fusiform face area (FFA) bilaterally and in the right lateral occipital area (LOC), but not in the occipital face area (OFA), suggesting their different roles in sensory competition. When we increased the spatial distance among pairs of faces the magnitude of suppressive interactions was reduced in the FFA. Surprisingly, the magnitude of competition depended on the visual hemifield of the stimuli: ipsilateral stimulation reduced the competition effects somewhat in the right LOC while it increased them in the left LOC. This suggests a left hemifield dominance of sensory competition. Our results support the sensory competition theory in the processing of multiple faces and suggests that sensory competition occurs in several cortical areas in both cerebral hemispheres.     

Selectivity of Face Perception to Horizontal Information over Lifespan (from 6 to 74 Year Old)

Face recognition in young human adults preferentially relies on the processing of horizontally-oriented visual information. We addressed whether the horizontal tuning of face perception is modulated by the extensive experience humans acquire with faces over the lifespan, or whether it reflects an invariable processing bias for this visual category. We tested 296 subjects aged from 6 to 74 years in a face matching task. Stimuli were upright and inverted faces filtered to preserve information in the horizontal or vertical orientation, or both (HV) ranges. The reliance on face-specific processing was inferred based on the face inversion effect (FIE). FIE size increased linearly until young adulthood in the horizontal but not the vertical orientation range of face information. These findings indicate that the protracted specialization of the face processing system relies on the extensive experience humans acquire at encoding the horizontal information conveyed by upright faces.     

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.     

Cortical responses to invisible faces: dissociating subsystems for facial-information processing

Perceiving faces is critical for social interaction. Evidence suggests that different neural pathways may be responsible for processing face identity and expression information. By using functional magnetic resonance imaging (fMRI), we measured brain responses when observers viewed neutral, fearful, and scrambled faces, either visible or rendered invisible through interocular suppression. The right fusiform face area (FFA), the right superior temporal sulcus (STS), and the amygdala responded strongly to visible faces. However, when face images became invisible, activity in FFA to both neutral and fearful faces was much reduced, although still measurable; activity in the STS was robust only to invisible fearful faces but not to neutral faces. Activity in the amygdala was equally strong in both the visible and invisible conditions to fearful faces but much weaker in the invisible condition for the neutral faces. In the invisible condition, amygdala activity was highly correlated with that of the STS but not with FFA. The results in the invisible condition support the existence of dissociable neural systems specialized for processing facial identity and expression information. When images are invisible, cortical responses may reflect primarily feed-forward visual-information processing and thus allow us to reveal the distinct functions of FFA and STS.     

Discriminating grotesque from typical faces: evidence from the Thatcher illusion

The discrimination of thatcherized faces from typical faces was explored in two simultaneous alternative forced choice tasks. Reaction times (RTs) and errors were measured in a behavioural task. Brain activation was measured in an equivalent fMRI task. In both tasks, participants were tested with upright and inverted faces. Participants were also tested on churches in the behavioural task. The behavioural task confirmed the face specificity of the illusion (by comparing inversion effects for faces against churches) but also demonstrated that the discrimination was primarily, although not exclusively, driven by attending to eyes. The fMRI task showed that, relative to inverted faces, upright grotesque faces are discriminated via activation of a network of emotion/social evaluation processing areas. On the other hand, discrimination of inverted thatcherized faces was associated with increased activation of brain areas that are typically involved in perceptual processing of faces.     

No about face on houses in the fusiform face area!

Yovel and Kanwisher (this issue of Neuron) altered upright and inverted face and house characteristics during a same-different task. The right fusiform face area (FFA) was more active to faces than houses but, unlike behavior, was unaffected by spatial configuration or parts manipulations. These data raise interesting questions regarding the relationship of brain activation to observed behavior.     

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.     

Early category-specific cortical activation revealed by visual stimulus inversion

Visual categorization may already start within the first 100-ms after stimulus onset, in contrast with the long-held view that during this early stage all complex stimuli are processed equally and that category-specific cortical activation occurs only at later stages. The neural basis of this proposed early stage of high-level analysis is however poorly understood. To address this question we used magnetoencephalography and anatomically-constrained distributed source modeling to monitor brain activity with millisecond-resolution while subjects performed an orientation task on the upright and upside-down presented images of three different stimulus categories: faces, houses and bodies. Significant inversion effects were found for all three stimulus categories between 70-100-ms after picture onset with a highly category-specific cortical distribution. Differential responses between upright and inverted faces were found in well-established face-selective areas of the inferior occipital cortex and right fusiform gyrus. In addition, early category-specific inversion effects were found well beyond visual areas. Our results provide the first direct evidence that category-specific processing in high-level category-sensitive cortical areas already takes place within the first 100-ms of visual processing, significantly earlier than previously thought, and suggests the existence of fast category-specific neocortical routes in the human brain.     

Own-Race Faces Capture Attention Faster than Other-Race Faces: Evidence from Response Time and the N2pc

Studies have shown that people are better at recognizing human faces from their own-race than from other-races, an effect often termed the Own-Race Advantage. The current study investigates whether there is an Own-Race Advantage in attention and its neural correlates. Participants were asked to search for a human face among animal faces. Experiment 1 showed a classic Own-Race Advantage in response time both for Chinese and Black South African participants. Using event-related potentials (ERPs), Experiment 2 showed a similar Own-Race Advantage in response time for both upright faces and inverted faces. Moreover, the latency of N2pc for own-race faces was earlier than that for other-race faces. These results suggested that own-race faces capture attention more efficiently than other-race faces.     

Abnormal FMRI adaptation to unfamiliar faces in a case of developmental prosopamnesia

In rare cases, damage to the temporal lobe causes a selective impairment in the ability to learn new faces, a condition known as prosopamnesia [1]. Here we present the case of an individual with prosopamnesia in the absence of any acquired structural lesion. "C" shows intact processing of simple and complex nonface objects, but her ability to learn new faces is severely impaired. We used a neural marker of perceptual learning known as repetition suppression to examine functioning within C's fusiform face area (FFA), a region of cortex involved in face perception [2]. For comparison, we examined repetition suppression in the scene-selective parahippocampal place area (PPA) [3]. As expected, normal controls showed significant region-specific attenuation of neural activity across repetitions of each stimulus class. C also showed normal attenuation within the PPA to familiar and unfamiliar scenes, and within the FFA to familiar faces. Critically, however, she failed to show any adaptive change within the FFA for repeated unfamiliar faces, despite a face-specific blood-oxygen-dependent response (BOLD) response in her FFA during viewing of face stimuli. Our findings suggest that in developmental prosopamnesia, the FFA cannot maintain stable representations of new faces for subsequent recall or recognition.     

TMS evidence for the involvement of the right occipital face area in early face processing

Extensive research has demonstrated that several specialized cortical regions respond preferentially to faces. One such region, located in the inferior occipital gyrus, has been dubbed the occipital face area (OFA). The OFA is the first stage in two influential face-processing models, both of which suggest that it constructs an initial representation of a face, but how and when it does so remains unclear. The present study revealed that repetitive transcranial magnetic stimulation (rTMS) targeted at the right OFA (rOFA) disrupted accurate discrimination of face parts but had no effect on the discrimination of spacing between these parts. rTMS to left OFA had no effect. A matched part and spacing discrimination task that used house stimuli showed no impairment. In a second experiment, rTMS to rOFA replicated the face-part impairment but did not produce the same effect in an adjacent area, the lateral occipital cortex. A third experiment delivered double pulses of TMS separated by 40 ms at six periods after stimulus presentation during face-part discrimination. Accuracy dropped when pulses were delivered at 60 and 100 ms only. These findings indicate that the rOFA processes face-part information at an early stage in the face-processing stream.