Corentin Jacques

Electrical Stimulation of Human Fusiform Face-Selective Regions Distorts Face Perception

Face-selective neural responses in the human fusiform gyrus have been widely examined. However, their causal role in human face perception is largely unknown. Here, we used a multimodal approach of electrocorticography (ECoG), high-resolution functional magnetic resonance imaging (fMRI), and electrical brain stimulation (EBS) to directly investigate the causal role of face-selective neural responses of the fusiform gyrus (FG) in face perception in a patient implanted with subdural electrodes in the right inferior temporal lobe. High-resolution fMRI identified two distinct FG face-selective regions [mFus-faces and pFus-faces (mid and posterior fusiform, respectively)]. ECoG revealed a striking anatomical and functional correspondence with fMRI data where a pair of face-selective electrodes, positioned 1 cm apart, overlapped mFus-faces and pFus-faces, respectively. Moreover, electrical charge delivered to this pair of electrodes induced a profound face-specific perceptual distortion during viewing of real faces. Specifically, the subject reported a “metamorphosed” appearance of faces of people in the room. Several controls illustrate the specificity of the effect to the perception of faces. EBS of mFus-faces and pFus-faces neither produced a significant deficit in naming pictures of famous faces on the computer, nor did it affect the appearance of nonface objects. Further, the appearance of faces remained unaffected during both sham stimulation and stimulation of a pair of nearby electrodes that were not face-selective. Overall, our findings reveal a striking convergence of fMRI, ECoG, and EBS, which together offer a rare causal link between functional subsets of the human FG network and face perception.

The Speed of Individual Face Categorization

How fast does the human visual system discriminate individual faces? To address this question, we used a continuous-stimulation paradigm in which event-related potentials (ERPs) to a face stimulus are recorded with respect to another face stimulus, rather than to a preceding blank-screen baseline epoch. Following the shift between two face stimuli, posterior sites showed an early negative ERP deflection that started at 130 ms and peaked at 160 ms, the latency of the N170, an ERP component associated with discriminating faces from objects. The ERP we recorded was larger in amplitude when the preceding stimulus was perceived as a different individual face rather than the same individual face, although face pairs were of equal physical distance in the two conditions. These findings provide direct evidence that individual face discrimination in humans can take place as early as 130 ms following stimulus onset, during the same time window as face detection.

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

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

Early adaptation to repeated unfamiliar faces across viewpoint changes in the right hemisphere : evidence from the N170 ERP component

Event-related potential (ERP) studies have shown that sensitivity to individual faces emerges as early as approximately 160ms in the human occipitotemporal cortex (N170). Here we tested whether this effect generalizes across changes in viewpoint. We recorded ERPs during an unfamiliar individual face adaptation paradigm. Participants were presented first with an adapting face ( approximately 3000ms) rotated 30 degrees in depth, followed by a second face (200ms) in a frontal view of either the same or a different identity. The N170 amplitude at right occipitotemporal sites to the second stimulus was reduced for repeated as compared to different faces. A bilateral adaptation effect emerged after 250ms following stimulus onset. These observations indicate that individual face representations activated as early as 160ms after stimulus onset in the right hemisphere show a substantial degree of generalization across viewpoints.

The initial representation of individual faces in the right occipito-temporal cortex is holistic: Electrophysiological evidence from the composite face illusion

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.

Diagnostic colours contribute to the early stages of scene categorization: Behavioural and neurophysiological evidence

We examined the effects of colour cues on the express categorization of natural scenes. Using a go/no-go paradigm sensitive to fast recognition processes, we measured early event-related potential (ERP) correlates of scene categorization to elucidate the processing stage at which colour contributes to scene recognition. Observers were presented with scenes belonging to four colour-diagnostic categories (desert, forest, canyon and coastline). Scenes were presented in one of three forms: Diagnostically coloured, nondiagnostically coloured, or greyscale images. In a verification task, observers were instructed to respond whenever the presented stimulus matched a previously presented category name. Reaction times and accuracy were optimal when the stimuli were presented as their original diagnostically coloured version, followed by their greyscale version, and lastly by their nondiagostically coloured version. These effects were mirrored in the early (i.e., 150 ms following stimulus onset) ERP frontal correlates. Their onset was delayed for greyscale scenes compared to diagnostically coloured scenes, and for nondiagnostically coloured scenes compared to the other two conditions. Frontal ERP amplitudes also decreased for greyscale and nondiagnostically coloured scenes. Together, the results suggest that diagnostic colours are part of the scene gist responsible for express scene categorization.

Early Visually Evoked Electrophysiological Responses Over the Human Brain (P1, N170) Show Stable Patterns of Face-Sensitivity from 4 years to Adulthood.

Whether the development of face recognition abilities truly reflects changes in how faces, specifically, are perceived, or rather can be attributed to more general perceptual or cognitive development, is debated. Event-related potential (ERP) recordings on the scalp offer promise for this issue because they allow brain responses to complex visual stimuli to be relatively well isolated from other sensory, cognitive and motor processes. ERP studies in 5- to 16-year-old children report large age-related changes in amplitude, latency (decreases) and topographical distribution of the early visual components, the P1 and the occipito-temporal N170. To test the face specificity of these effects, we recorded high-density ERPs to pictures of faces, cars, and their phase-scrambled versions from 72 children between the ages of 4 and 17, and a group of adults. We found that none of the previously reported age-dependent changes in amplitude, latency or topography of the P1 or N170 were specific to faces. Most importantly, when we controlled for age-related variations of the P1, the N170 appeared remarkably similar in amplitude and topography across development, with much smaller age-related decreases in latencies than previously reported. At all ages the N170 showed equivalent face-sensitivity: it had the same topography and right hemisphere dominance, it was absent for meaningless (scrambled) stimuli, and larger and earlier for faces than cars. The data also illustrate the large amount of inter-individual and inter-trial variance in young childrens data, which causes the N170 to merge with a later component, the N250, in grand-averaged data. Based on our observations, we suggest that the previously reported “bi-fid” N170 of young children is in fact the N250. Overall, our data indicate that the electrophysiological markers of face-sensitive perceptual processes are present from 4 years of age and do not appear to change throughout development.

Controlling interstimulus perceptual variance does not abolish N170 face sensitivity.

Numerous studies report a negative event-related potential at occipito-temporal scalp sites between 130 and 200 ms (N170) that is larger when elicited by faces than by other object categories. Thierry and colleagues argued that this effect reflects an artifact of uncontrolled interstimulus perceptual (physical) variance (ISPV), which when controlled eliminates the difference between faces and nonfaces.

Electrical stimulation of the left and right human fusiform gyrus causes different effects in conscious face perception.

Neuroimaging and electrophysiological studies across species have confirmed bilateral face-selective responses in the ventral temporal cortex (VTC) and prosopagnosia is reported in patients with lesions in the VTC including the fusiform gyrus (FG). As imaging and electrophysiological studies provide correlative evidence, and brain lesions often comprise both white and gray matter structures beyond the FG, we designed the current study to explore the link between face-related electrophysiological responses in the FG and the causal effects of electrical stimulation of the left or right FG in face perception. We used a combination of electrocorticography (ECoG) and electrical brain stimulation (EBS) in 10 human subjects implanted with intracranial electrodes in either the left (5 participants, 30 FG sites) or right (5 participants, 26 FG sites) hemispheres. We identified FG sites with face-selective ECoG responses, and recorded perceptual reports during EBS of these sites. In line with existing literature, face-selective ECoG responses were present in both left and right FG sites. However, when the same sites were stimulated, we observed a striking difference between hemispheres. Only EBS of the right FG caused changes in the conscious perception of faces, whereas EBS of strongly face-selective regions in the left FG produced non-face-related visual changes, such as phosphenes. This study examines the relationship between correlative versus causal nature of ECoG and EBS, respectively, and provides important insight into the differential roles of the right versus left FG in conscious face perception.

Concurrent processing reveals competition between visual representations of faces

Scalp electrophysiological recordings in humans indicate that the processing of faces differs from other categories between 100 and 200 ms after stimulus onset, peaking at the N170. To test the effect of the addition of a second face stimulus in the visual field on the face-related N170, we measured this component in response to a laterally presented face stimulus while subjects were processing either a central face or a control stimulus. As early as 130 ms following the lateralized face stimulus, there was a strong (∼40% of signal) and specific reduction of the N170 amplitude when subjects were concurrently processing a central face. This observation suggests that the early stages of the N170 reflect the activation of individual faces having overlapping and competing neural representations in the human occipito-temporal cortex.