Nicolas Burra

Amygdala Activation for Eye Contact Despite Complete Cortical Blindness

Cortical blindness refers to the loss of vision that occurs after destruction of the primary visual cortex. Although there is no sensory cortex and hence no conscious vision, some cortically blind patients show amygdala activation in response to facial or bodily expressions of emotion. Here we investigated whether direction of gaze could also be processed in the absence of any functional visual cortex. A well-known patient with bilateral destruction of his visual cortex and subsequent cortical blindness was investigated in an fMRI paradigm during which blocks of faces were presented either with their gaze directed toward or away from the viewer. Increased right amygdala activation was found in response to directed compared with averted gaze. Activity in this region was further found to be functionally connected to a larger network associated with face and gaze processing. The present study demonstrates that, in human subjects, the amygdala response to eye contact does not require an intact primary visual cortex.

Attentional capture during visual search is attenuated by target predictability: Evidence from the N2pc, Pd, and topographic segmentation

Attentional capture by salient distractors has been confirmed by the occurrence of an N2pc to the salient distractor. To clarify some failures to replicate this finding, we varied target predictability to induce different search modes. In the unpredictable target condition, the target shape varied randomly from trial to trial, favoring singleton detection mode. In the predictable target condition, the target shape remained the same in a block of trials, favoring feature search mode. With unpredictable targets, we observed an N2pc toward the salient color distractor, confirming attentional capture in singleton search mode. With predictable targets, there was no N2pc to the salient distractor, but a distractor positivity (Pd), suggesting distractor suppression. Also, differences emerged in the topographic segmentation of N2pc and Pd. Further, the amplitude of the N2pc toward the target was larger with predictable than with unpredictable targets.

The distractor positivity (Pd) signals lowering of attentional priority: Evidence from event-related potentials and individual differences

We investigated the effects of task demands and individual differences on the allocation of attention. Using the same stimuli, participants indicated the orientation of a line contained in a shape singleton (identification task) or the presence of singletons (detection task). Shape singletons in the identification task elicited a contralateral negativity (N2pc) whereas shape singletons in the detection task elicited a contralateral positivity (Pd). We suggest that the reduction of attentional priority of a salient stimulus, reflected by the Pd, occurred more rapidly with the less demanding detection task. Further, fewer distractible participants showed a larger N2pc to lateral color distractors than highly distractible participants. We suggest that highly distractible participants developed compensatory mechanisms to suppress distracting stimuli.

Affective blindsight relies on low spatial frequencies

The human brain can process facial expressions of emotions rapidly and without awareness. Several studies in patients with damage to their primary visual cortices have shown that they may be able to guess the emotional expression on a face despite their cortical blindness. This non-conscious processing, called affective blindsight, may arise through an intact subcortical visual route that leads from the superior colliculus to the pulvinar, and thence to the amygdala. This pathway is thought to process the crude visual information conveyed by the low spatial frequencies of the stimuli. In order to investigate whether this is the case, we studied a patient (TN) with bilateral cortical blindness and affective blindsight. An fMRI paradigm was performed in which fearful and neutral expressions were presented using faces that were either unfiltered, or filtered to remove high or low spatial frequencies. Unfiltered fearful faces produced right amygdala activation although the patient was unaware of the presence of the stimuli. More importantly, the low spatial frequency components of fearful faces continued to produce right amygdala activity while the high spatial frequency components did not. Our findings thus confirm that the visual information present in the low spatial frequencies is sufficient to produce affective blindsight, further suggesting that its existence could rely on the subcortical colliculo-pulvino-amygdalar pathway.

Electrophysiological evidence for attentional capture by irrelevant angry facial expressions.

Attention is believed to be biased toward threatening objects or faces. Therefore, we tested whether angry face stimuli would capture attention even when they are irrelevant to the task. Observers searched for a neutral face with a tilted nose. On some trials, the target was shown together with an irrelevant angry or happy face and we measured the N2pc (an electrophysiological marker of attentional selectivity) to

Lack of automatic attentional orienting by gaze cues following a bilateral loss of visual cortex.

In social interactions, the location of relevant stimuli is often indicated by the orientation of gaze. It has been proposed that the direction of gaze might produce an automatic cueing of attention, similar to what is observed with exogenous cues. However, several reports have challenged this claim by demonstrating that the behavioral gain that arises with gaze cueing could be explained by shifts of attention, which are intentional and not automatic. We reasoned that if cueing by gaze was truly automatic, it should occur without awareness and should be sustained by subcortical circuits, including the amygdalae, independently of the main geniculo-striate visual pathway. We presented a cross-modal version of the Posner cueing paradigm to a patient (TN) with bilateral lesions of occipital cortex (Burra et al., 2013; Pegna, Khateb, Lazeyras, & Seghier, 2005). TN was asked to localize a sound using a key press. The location of the sound was congruent or incongruent with the direction of gaze of a face-cue. In groups of healthy young and age-matched participants, we observed significantly longer response times for incongruent than congruent sounds, suggesting that gaze direction interfered with processing of localized sounds. By contrast, TN׳s performance was not affected by sound-gaze congruence. The results suggest that the processing of gaze orientation cannot occur in the absence of geniculo-striate processing, suggesting that it is not automatic.

Saliency Changes Appearance

Numerous studies have suggested that the deployment of attention is linked to saliency. In contrast, very little is known about how salient objects are perceived. To probe the perception of salient elements, observers compared two horizontally aligned stimuli in an array of eight elements. One of them was salient because of its orientation or direction of motion. We observed that the perceived luminance contrast or color saturation of the salient element increased: the salient stimulus looked even more salient. We explored the possibility that changes in appearance were caused by attention. We chose an event-related potential indexing attentional selection, the N2pc, to answer this question. The absence of an N2pc to the salient object provides preliminary evidence against involuntary attentional capture by the salient element. We suggest that signals from a master saliency map flow back into individual feature maps. These signals boost the perceived feature contrast of salient objects, even on perceptual dimensions different from the one that initially defined saliency.

Straight gaze facilitates face processing but does not cause involuntary attentional capture

ABSTRACT This study aimed to investigate the conditions under which eyes with a straight gaze capture attention more than eyes with an averted gaze, a phenomenon called the stare-in-the-crowd effect. In Experiment 1, we measured attentional capture by distractor faces with either straight or averted gaze that were shown among faces with closed eyes. Gaze direction of the distractor face was irrelevant because participants searched for a tilted face and indicated its gender. The presence of the distractor face with open eyes resulted in slower reaction times, but gaze direction had no effect, suggesting that straight gaze does not result in more involuntary attentional capture than averted gaze. In three further experiments with the same stimuli, the gaze direction of the target, and not the distractor, was varied. Better performance with straight than averted gaze of the target face was observed when the gaze direction or gender of the target face had to be discriminated. However, no difference between straight and averted was observed when only the presence of a face with open eyes had to be detected. Thus, the stare-in-the crowd effect is only observed when eye gaze is selected as part of the target and only when features of the face have to be discriminated. Our findings suggest that preference for straight gaze bears on target-related processes rather than on attentional capture per se.

Early Left Parietal Activity Elicited by Direct Gaze: A High-Density EEG Study.

Gaze is one of the most important cues for human communication and social interaction. In particular, gaze contact is the most primary form of social contact and it is thought to capture attention. A very early-differentiated brain response to direct versus averted gaze has been hypothesized. Here, we used high-density electroencephalography to test this hypothesis. Topographical analysis allowed us to uncover a very early topographic modulation (40–80 ms) of event-related responses to faces with direct as compared to averted gaze. This modulation was obtained only in the condition where intact broadband faces–as opposed to high-pass or low-pas filtered faces–were presented. Source estimation indicated that this early modulation involved the posterior parietal region, encompassing the left precuneus and inferior parietal lobule. This supports the idea that it reflected an early orienting response to direct versus averted gaze. Accordingly, in a follow-up behavioural experiment, we found faster response times to the direct gaze than to the averted gaze broadband faces. In addition, classical evoked potential analysis showed that the N170 peak amplitude was larger for averted gaze than for direct gaze. Taken together, these results suggest that direct gaze may be detected at a very early processing stage, involving a parallel route to the ventral occipito-temporal route of face perceptual analysis.

Electrophysiological evidence for attentional capture by irrelevant angry facial expressions: Naturalistic faces

Recently, research on lateralized event related potentials (ERPs) in response to irrelevant distractors has revealed that angry but not happy schematic distractors capture spatial attention. Whether this effect occurs in the context of the natural expression of emotions is unknown. To fill this gap, observers were asked to judge the gender of a natural face surrounded by a color singleton among five other face identities. In contrast to previous studies, the similarity between the task-relevant feature (color) and the distractor features was low. On some trials, the target was displayed concurrently with an irrelevant angry or happy face. The lateralized ERPs to these distractors were measured as a marker of spatial attention. Our results revealed that angry face distractors, but not happy face distractors, triggered a PD, which is a marker of distractor suppression. Subsequent to the PD, angry distractors elicited a larger N450 component, which is associated with conflict detection. We conclude that threatening expressions have a high attentional priority because of their emotional value, resulting in early suppression and late conflict detection.