Neurotypical human adults have a high level of expertise in facial recognition, a key brain function for the quality of their social interactions. Studying cerebral mechanisms of facial recognition ...should help us understanding the most complex mechanisms of perception, memory, learning, as well as integration of semantic knowledge, emotion and attention in the brain. Neurophysiological studies performed in the macaque monkey brain are usually taken as providing evidence for the mechanisms of human face recognition but their relevance is limited by the weak capacities of this species in facial recognition compared to humans, and the absence of a human-like ventral occipito-temporal circuit selectively involved in face recognition. Functional magnetic resonance imaging studies in humans have identified a large network of occipito-temporal face-selective regions, dominant in the right hemisphere, but are limited in their temporal resolution and by important variations of signal in this region. By coupling electrophysiological recordings on large sample of human brain implanted with stereoélectroencephalography (SEEG) with fast periodic visual stimulation, this presentation will show how we can objectively and rapidly map human facial recognition in the human ventral temporal lobe, in order to make significant progress in our understanding of this function.
(1) To investigate the hypothesis that the vertex positive potential (VPP) and the N170 ERP components reported in the face processing literature are two manifestations of the same brain processes ...whose relative amplitude in a given experiment is dependent on reference electrode; (2) to investigate whether differences in face/object results reported in studies looking at the VPP and N170 are attributable to the location of reference.
EEG was recorded from 53 scalp electrodes referenced online to the left mastoid while subjects viewed face, car and word stimuli. Off-line, the data were systematically re-referenced to the common average, averaged mastoids, averaged earlobes, non-cephalic, and nose. The correlation of timing, amplitude, and effects was investigated across reference electrodes.
(1) The amplitude of the N170 and VPP components varies in a precisely inverse manner across reference; (2) the peaks of the N170 and VPP are temporally coincident for all reference electrodes, (3) both components can be accounted for by the same dipolar configuration, and (4) the components show identical functional properties.
The VPP and N170 are two ‘faces’ of the same brain generators.
The differential N170/VPP effects observed in ERP studies can be accounted for by differences in reference methodology.
Understanding how the human brain discriminates complex visual patterns, such as individual faces, is an important issue in Vision Science. Here we tested sensitivity to individual faces using ...steady-state visual-evoked potentials (SSVEPs). Twelve participants were presented with 90-s sequences of faces appearing at a constant rate (3.5 faces/s) while high-density electroencephalogram (EEG) was recorded. Fast Fourier Transform (FFT) of EEG showed a large response at the fundamental stimulation frequency (3.5 Hz) over posterior electrode sites. This response was much larger when the face identity changed at that rate (different faces) than when an identical face was repeated. The reduction of signal in the identical face condition was not due to low-level feature adaptation, since it was observed despite changes of stimulus size, and was localized specifically over the right lateral occipital cortex. Moreover, the difference between conditions disappeared when faces were inverted. This first observation of habituation of the SSVEP to repeated face identity in the human brain provides further evidence for face individualization in the right occipito-temporal cortex by means of a simple, fast, and high signal-to-noise approach. Most importantly, it offers a promising tool to study the sensitivity to visual features of individual faces and objects in the human brain.
•FPVS allows high-SNR EEG/MEG recordings of face-selective brain responses.•High comparable z-scores obtained for EEG and MEG in all but one participants.•Face-selective responses right-lateralized ...in EEG.•Face-selective responses bilateral but numerically right-lateralized in MEG.•Strongest face-selective sources anterior to base frequency response.
Fast periodic visual stimulation (FPVS) allows the recording of objective brain responses of human face categorization (i.e., generalizable face-selective responses) with high signal-to-noise ratio. This approach has been successfully employed in a number of scalp electroencephalography (EEG) studies but has not been used with magnetoencephalography (MEG) yet, let alone with combined MEG/EEG recordings and distributed source estimation. Here, we presented various natural images of faces periodically (1.2 Hz) among natural images of objects (base frequency 6 Hz) whilst recording simultaneous EEG and MEG in 15 participants. Both measurement modalities showed face-selective responses at 1.2 Hz and harmonics across participants, with high and comparable signal-to-noise ratio (SNR) in about 3 min of stimulation. The correlation of face categorization responses between EEG and two MEG sensor types was lower than between the two MEG sensor types, indicating that the two sensor modalities provide independent information about the sources of face-selective responses. Face-selective EEG responses were right-lateralized as reported previously, and were numerically but non-significantly right-lateralized in MEG data. Distributed source estimation based on combined EEG/MEG signals confirmed a more bilateral face-selective response in visual brain regions located anteriorly to the common response to all stimuli at 6 Hz and harmonics. Conventional sensor and source space analyses of evoked responses in the time domain further corroborated this result. Our results demonstrate that FPVS in combination with simultaneously recorded EEG and MEG may serve as an efficient localizer paradigm for human face categorization.
Neuroimaging studies have identified at least two bilateral areas of the visual extrastriate cortex that respond more to pictures of faces than objects in normal human subjects in the middle fusiform ...gyrus the ‘fusiform face area’ (FFA) and, more posteriorly, in the inferior occipital cortex ‘occipital face area’ (OFA), with a right hemisphere dominance. However, it is not yet clear how these regions interact which each other and whether they are all necessary for normal face perception. It has been proposed that the right hemisphere FFA acts as an isolated (‘modular’) processing system for faces or that this region receives its face‐sensitive inputs from the OFA in a feedforward hierarchical model of face processing. To test these proposals, we report a detailed neuropsychological investigation combined with a neuroimaging study of a patient presenting a deficit restricted to face perception, consecutive to bilateral occipito‐temporal lesions. Due to the asymmetry of the lesions, the left middle fusiform gyrus and the right inferior occipital cortex were damaged but the right middle fusiform gyrus was structurally intact. Using functional MRI, we disclosed a normal activation of the right FFA in response to faces in the patient despite the absence of any feedforward inputs from the right OFA, located in a damaged area of cortex. Together, these findings show that the integrity of the right OFA is necessary for normal face perception and suggest that the face‐sensitive responses observed at this level in normal subjects may arise from feedback connections from the right FFA. In agreement with the current literature on the anatomical basis of prosopagnosia, it is suggested that the FFA and OFA in the right hemisphere and their re‐entrant integration are necessary for normal face processing.
Identifying a facial feature (e.g. the eyes) is influenced by the position and identity of other features (e.g. the mouth) of the face, supporting the view that an individual face is represented as a ...whole in the human brain. To clarify how early in the time-course of face processing this holistic individual representation is accessed we recorded event-related potentials during an adaptation paradigm of the composite face illusion (CFI). Observers performed a matching task on top halves of two faces presented sequentially. For each face pair, top and bottom face halves could be both identical, both different, or only the bottom half differed. The signal was larger over the right occipito-temporal cortex at about 160 ms (N170) when the attended top half differed between the two faces than when identical top halves were repeated. Crucially, a larger N170 was also found when the top halves of the two faces were the same, yet the observers had the illusion that they differed (CFI). This effect was not found when the two face halves were spatially misaligned. These observations indicate that the earliest perceptual representation of an individual face in the human brain is holistic rather than based on independent face parts.
Highlights ► Transient prosopagnosia from human brain intracerebral stimulation is reported. ► The recognition impairment is specific to faces. ► The area stimulated is functionally defined as the ...right ‘occipital face area’. ► A face-sensitive N170 potential is recorded directly in this area.
Whether and how the parts of a visual object are grouped together to form an integrated ("holistic") representation is a central question in cognitive neuroscience. Although the face is considered to ...be the quintessential example of holistic representation, this issue has been the subject of much debate in face perception research. The implication of holistic processing is that the response to the whole cannot be predicted from the sum of responses to the parts. Here we apply techniques from nonlinear systems analysis to provide an objective measure of the nonlinear integration of parts into a whole, using the left and right halves of a face stimulus as the parts. High-density electroencephalogram (EEG) was recorded in 15 human participants presented with two halves of a face stimulus, flickering at different frequencies (5.88 vs. 7.14 Hz). Besides specific responses at these fundamental frequencies, reflecting part-based responses, we found intermodulation components (e.g., 7.14 - 5.88 = 1.26 Hz) over the right occipito-temporal hemisphere, reflecting nonlinear integration of the face halves. Part-based responses did not depend on the relative alignment of the two face halves, their spatial separation, or whether the face was presented upright or inverted. By contrast, intermodulations were virtually absent when the two halves were spatially misaligned and separated. Inversion of the whole face configuration also reduced specifically the intermodulation components over the right occipito-temporal cortex. These observations indicate that the intermodulation components constitute an objective, configuration-specific signature of an emergent neural representation of the whole face that is distinct from that generated by the parts themselves.
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.
Human face perception requires a network of brain regions distributed throughout the occipital and temporal lobes with a right hemisphere advantage. Present theories consider this network as either a ...processing hierarchy beginning with the inferior occipital gyrus (occipital face area; IOG-faces/OFA) or a multiple-route network with nonhierarchical components. The former predicts that removing IOG-faces/OFA will detrimentally affect downstream stages, whereas the latter does not. We tested this prediction in a human patient (Patient S.P.) requiring removal of the right inferior occipital cortex, including IOG-faces/OFA. We acquired multiple fMRI measurements in Patient S.P. before and after a preplanned surgery and multiple measurements in typical controls, enabling both within-subject/across-session comparisons (Patient S.P. before resection vs Patient S.P. after resection) and between-subject/across-session comparisons (Patient S.P. vs controls). We found that the spatial topology and selectivity of downstream ipsilateral face-selective regions were stable 1 and 8 month(s) after surgery. Additionally, the reliability of distributed patterns of face selectivity in Patient S.P. before versus after resection was not different from across-session reliability in controls. Nevertheless, postoperatively, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1 of the resected hemisphere. Diffusion weighted imaging in Patient S.P. and controls identifies white matter tracts connecting retinotopic areas to downstream face-selective regions, which may contribute to the stable and plastic features of the face network in Patient S.P. after surgery. Together, our results support a multiple-route network of face processing with nonhierarchical components and shed light on stable and plastic features of high-level visual cortex following focal brain damage.
Brain networks consist of interconnected functional regions commonly organized in processing hierarchies. Prevailing theories predict that damage to the input of the hierarchy will detrimentally affect later stages. We tested this prediction with multiple brain measurements in a rare human patient requiring surgical removal of the putative input to a network processing faces. Surprisingly, the spatial topology and selectivity of downstream face-selective regions are stable after surgery. Nevertheless, representations of visual space were typical in dorsal face-selective regions but atypical in ventral face-selective regions and V1. White matter connections from outside the face network may support these stable and plastic features. As processing hierarchies are ubiquitous in biological and nonbiological systems, our results have pervasive implications for understanding the construction of resilient networks.
PDF
