Nathalie George

Perception's shadow: long-distance synchronization of human brain activity

Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30–80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea (see, for example, refs 4,5,6,7,8,9,10). In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography and magnetoencephalography) and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.

Seen Gaze-Direction Modulates Fusiform Activity and Its Coupling with Other Brain Areas during Face Processing

Gaze-contact is often a preliminary to social interaction and so constitutes a signal for the allocation of processing resources to the gazing face. We investigated how gaze direction influences face processing in an fMRI study, where seen gaze and head direction could independently be direct or deviated. Direct relative to averted gaze elicited stronger activation for faces in ventral occipitotemporal cortices around the fusiform gyrus, regardless of head orientation. Moreover, direct gaze led to greater correlation between activity in the fusiform and the amygdala, a region associated with emotional responses and stimulus saliency. By contrast, faces with averted gaze (again, regardless of head orientation) yielded increased correlation between activity in the fusiform and the intraparietal sulcus, a region associated with shifting attention to the periphery.

The many faces of the gamma band response to complex visual stimuli.

While much is known about the functional architecture of the visual system, little is known about its large-scale dynamics during perception. This study describes this dynamics with a high spatial, temporal and spectral resolution. We recorded depth EEG of epileptic patients performing a face detection task and found that the stimuli induced strong modulations in the gamma band (40 Hz to 200 Hz) in selective occipital, parietal and temporal sites, in particular the fusiform gyrus, the lateral occipital gyrus and the intra-parietal sulcus. Occipito-temporal sites were the first to be activated, closely followed by the parietal sites, while portions of the primary visual cortex seemed to deactivate temporarily. Some of those effects were found to be correlated across distant sites, suggesting that a coordinated balance between regional gamma activations and deactivations could be involved during visual perception.

Contrast polarity and face recognition in the human fusiform gyrus

Functional imaging has revealed face-responsive visual areas in the human fusiform gyrus, but their role in recognizing familiar individuals remains controversial. Face recognition is particularly impaired by reversing contrast polarity of the image, even though this preserves all edges and spatial frequencies. Here, combined influences of familiarity and priming on face processing were examined as contrast polarity was manipulated. Our fMRI results show that bilateral posterior areas in fusiform gyrus responded more strongly for faces with positive than with negative contrast polarity. An anterior, right-lateralized fusiform region is activated when a given face stimulus becomes recognizable as a well-known individual.

Neural Network Involved in Time Perception: An fMRI Study Comparing Long and Short Interval Estimation

In this study, long (∼1,300 ms) and short duration (∼450 ms) estimation trials in an event‐related functional MRI (fMRI) study were contrasted in order to reveal the regions within a time estimation network yielding increased activation with the increase of the duration to be estimated. In accordance with numerous imaging studies, our results showed that the presupplementary motor area (preSMA), the anterior cingulate, the prefrontal and parietal cortices, and the basal ganglia were involved in the estimation trials whatever the duration to be estimated. Moreover, only a subset of the regions within this distributed cortical and subcortical network yielded increased activation with increasing time, namely, the preSMA, the anterior cingulate cortex, the right inferior frontal gyrus (homolog to Brocas area), the bilateral premotor cortex, and the right caudate nucleus. This suggests that these regions are directly involved in duration estimation. We propose that the caudate‐preSMA circuit, the anterior cingulate, and the premotor‐inferior frontal regions may support a clock mechanism, decision and response‐related processes, and active maintenance of temporal information, respectively. Hum. Brain Mapping, 2005.

When eye creates the contact! ERP evidence for early dissociation between direct and averted gaze motion processing

Direct gaze or eye contact is a strong social signal, which triggers distinct processes as compared to other gaze directions. Thus, direct gaze could be early dissociated from averted gaze during the processing of gaze direction. In order to examine the processing of gaze contact relative to averted gaze, we studied evoked potentials in human adults in response to the apparent motion of gaze. Deviated and frontal faces were presented with a fixed gaze direction, followed by an apparent movement of the eyes either toward the subject or away from him/her. The results showed that the perception of direct relative to averted gaze evoked a greater, later and longer lasting N170, suggesting that gaze contact recruited more resources than averted gaze in the early stage of gaze direction processing. Furthermore, direct and averted motion of gaze elicited distinct ERP components between 160 and 210 ms, initiated over centro-parietal electrodes. Source reconstruction revealed the involvement of the Theory-of-Mind network, including the regions of the superior temporal sulcus, the medial prefrontal and the orbitofrontal cortices, in this early dissociation. In addition, the perception of gaze contact relative to averted gaze yielded increased fronto-central P3a and parieto-occipital P3b. All the results were significant whatever the head orientation. Our findings show that gaze contact, as compared to other gaze directions, is an essential social cue which recruits early specific processes. The dissociation between direct and averted gaze processing occurs as soon as 160 ms, involving the social brain network.

Inversion and contrast-reversal effects on face processing assessed by MEG.

The processing of upright, inverted and contrast-reversed faces was investigated using MEG. Peak and global field power analyses revealed that the M100, M170 and M220 components were delayed for inverted and contrast-reversed compared to normal upright faces but no amplitude modulations were found. Source analyses using an event-related SAM beamformer technique revealed bilateral occipital sources for the M100 and M220 components. For the M170, two distinct sources simultaneously active were found, a bilateral and posterior source (M170A) and a right lateralized ventral and more anterior source (M170B) around the fusiform gyrus. None of the sources varied in location or intensity between face types. However, although different from the M100, the location of the M170A was not significantly different from that of the M220, suggesting the latter could be a reactivation of the former. Confirming previous ERP results on the processing of inverted faces, the present study extends the findings to contrast-reversed face stimuli and suggests that deviations from the standard upright face format do not activate extra areas but simply result in the delayed activation of the sources generating the M100, M170 and M220 components. The data confirm the sensitivity of the M100 to face manipulations and further suggest that the M170 is generated by two distinct sources, one of which situated in occipital extrastriate areas (M170A) could be reactivated around 220 ms to generate the M220 component.

Effects of perceived mutual gaze and gender on face processing and recognition memory

Perceived gaze contact in seen faces may convey important social signals. We examined whether gaze perception affects face processing during two tasks: Online gender judgement, and later incidental recognition memory. Individual faces were presented with eyes directed either straight towards the viewer or away, while these faces were seen in either frontal or three-quarters view. Participants were slower to make gender judgements for faces with direct versus averted eye gaze, but this effect was particularly pronounced for faces with opposite gender to the observer, and seen in three-quarters view. During subsequent surprise recognition-memory testing, recognition was better for faces previously seen with direct than averted gaze, again especially for the opposite gender to the observer. The effect of direct gaze was stronger in both tasks when the head was seen in three-quarters rather than in frontal view, consistent with the greater salience of perceived eye contact for deviated faces. However, in the memory test, face recognition was also relatively enhanced for faces of opposite gender in front views when their gaze was averted rather than direct. Together, these results indicate that perceived eye contact can interact with facial processing during gender judgements and recognition memory, even when gaze direction is task-irrelevant, and particularly for faces of opposite gender to the observer (an influence which controls for stimulus factors when considering observers of both genders). These findings appear consistent with recent neuroimaging evidence that social facial cues can modulate visual processing in cortical regions involved in face processing and memory, presumably via interconnections with brain systems specialized for gaze perception and social monitoring.

A meta-analysis of the anterior cingulate contribution to social pain

Many functional magnetic resonance imaging studies have explored the neural correlates of social pain that results from social threat, exclusion, rejection, loss or negative evaluation. Although activations have consistently been reported within the anterior cingulate cortex (ACC), it remains unclear which ACC subdivision is particularly involved. To provide a quantitative estimation of the specific involvement of ACC subdivisions in social pain, we conducted a voxel-based meta-analysis. The literature search identified 46 articles that included 940 subjects, the majority of which used the cyberball task. Significant likelihoods of activation were found in both the ventral and dorsal ACC for both social pain elicitation and self-reported distress during social pain. Self-reported distress involved more specifically the subgenual and pregenual ACC than social pain-related contrasts. The cyberball task involved the anterior midcingulate cortex to a lesser extent than other experimental tasks. During social pain, children exhibited subgenual activations to a greater extent than adults. Finally, the ventro-dorsal gradient of ACC activations in cyberball studies was related to the length of exclusion phases. The present meta-analysis contributes to a better understanding of the role of ACC subdivisions in social pain, and it could be of particular importance for guiding future studies of social pain and its neural underpinnings.

Magnetoencephalographic evidence of early processing of direction of gaze in humans

Despite the crucial importance of direction of gaze in social interactions, it is only recently that there has been interest in human brain responses to gaze direction. Using full-head magnetoencephalography, we investigated the correlates of direction of gaze in full faces and in eyes-only stimuli, measuring the early face-responsive component between 145 and 225 ms. Faces with eyes forward or averted had larger responses than faces with eyes up or closed. For eyes-only stimuli the shortest latencies were seen for eyes averted and the smallest amplitudes were seen for eyes closed. The data were explained by two dipoles in inferior-temporal regions, which showed greater activation for upright faces than face parts or inverted faces, as well as some sensitivity to direction of gaze in this very early stage of processing.