Intracortical recordings reveal vision-to-action cortical gradients driving human exogenous attention.

Exogenous attention, the process that makes external salient stimuli pop-out of a visual scene, is essential for survival. How attention-capturing events modulate human brain processing remains unclear. Here we show how the psychological construct of exogenous attention gradually emerges over large-scale gradients in the human cortex, by analyzing activity from 1,403 intracortical contacts implanted in 28 individuals, while they performed an exogenous attention task. The timing, location and task-relevance of attentional events defined a spatiotemporal gradient of three neural clusters, which mapped onto cortical gradients and presented a hierarchy of timescales. Visual attributes modulated neural activity at one end of the gradient, while at the other end it reflected the upcoming response timing, with attentional effects occurring at the intersection of visual and response signals. These findings challenge multi-step models of attention, and suggest that frontoparietal networks, which process sequential stimuli as separate events sharing the same location, drive exogenous attention phenomena such as inhibition of return.

Fronto-parietal networks shape human conscious report through attention gain and reorienting.

How do attention and consciousness interact in the human brain? Rival theories of consciousness disagree on the role of fronto-parietal attentional networks in conscious perception. We recorded neural activity from 727 intracerebral contacts in 13 epileptic patients, while they detected near-threshold targets preceded by attentional cues. Clustering revealed three neural patterns: first, attention-enhanced conscious report accompanied sustained right-hemisphere fronto-temporal activity in networks connected by the superior longitudinal fasciculus (SLF) II-III, and late accumulation of activity (>300 ms post-target) in bilateral dorso-prefrontal and right-hemisphere orbitofrontal cortex (SLF I-III). Second, attentional reorienting affected conscious report through early, sustained activity in a right-hemisphere network (SLF III). Third, conscious report accompanied left-hemisphere dorsolateral-prefrontal activity. Task modeling with recurrent neural networks revealed multiple clusters matching the identified brain clusters, elucidating the causal relationship between clusters in conscious perception of near-threshold targets. Thus, distinct, hemisphere-asymmetric fronto-parietal networks support attentional gain and reorienting in shaping human conscious experience.

The cost of attentional reorienting on conscious visual perception: an MEG study.

How do attentional networks influence conscious perception? To answer this question, we used magnetoencephalography in human participants and assessed the effects of spatially nonpredictive or predictive supra-threshold peripheral cues on the conscious perception of near-threshold Gabors. Three main results emerged. (i) As compared with invalid cues, both nonpredictive and predictive valid cues increased conscious detection. Yet, only predictive cues shifted the response criterion toward a more liberal decision (i.e. willingness to report the presence of a target under conditions of greater perceptual uncertainty) and affected target contrast leading to 50% detections. (ii) Conscious perception following valid predictive cues was associated to enhanced activity in frontoparietal networks. These responses were lateralized to the left hemisphere during attentional orienting and to the right hemisphere during target processing. The involvement of frontoparietal networks occurred earlier in valid than in invalid trials, a possible neural marker of the cost of re-orienting attention. (iii) When detected targets were preceded by invalid predictive cues, and thus reorienting to the target was required, neural responses occurred in left hemisphere temporo-occipital regions during attentional orienting, and in right hemisphere anterior insular and temporo-occipital regions during target processing. These results confirm and specify the role of frontoparietal networks in modulating conscious processing and detail how invalid orienting of spatial attention disrupts conscious processing.

How does reward compete with goal-directed and stimulus-driven shifts of attention?

In order to behave adaptively, attention can be directed in space either voluntarily (i.e. endogenously) according to strategic goals, or involuntarily (i.e. exogenously) through reflexive capture by salient or novel events. The emotional or motivational values of stimuli can also influence attentional orienting. However, little is known about how reward-related effects compete or interact with endogenous and exogenous attention mechanisms. Here we designed a visual search paradigm in which goal-driven and stimulus-driven shifts of attention were manipulated by classic spatial cueing procedures, while an irrelevant, but previously rewarded stimulus also appeared as a distractor and hence competed with both types of spatial attention during search. Our results demonstrated that stimuli previously associated with a high monetary reward received higher attentional priority in the subsequent visual search task, even though these stimuli and reward were no longer task-relevant, mitigating the attentional orienting induced by both endogenous and exogenous cues.

Interactions between phasic alerting and consciousness in the fronto-striatal network.

Only a small fraction of all the information reaching our senses can be the object of conscious report or voluntary action. Although some models propose that different attentional states (top-down amplification and vigilance) are necessary for conscious perception, few studies have explored how the brain activations associated with different attentional systems (such as top-down orienting and phasic alerting) lead to conscious perception of subsequent visual stimulation. The aim of the present study was to investigate the neural mechanisms associated with endogenous spatial attention and phasic alertness, and their interaction with the conscious perception of near-threshold stimuli. The only region demonstrating a neural interaction between endogenous attention and conscious perception was the thalamus, while a larger network of cortical and subcortical brain activations, typically associated with phasic alerting, was highly correlated with participants' conscious reports. Activation of the anterior cingulate cortex, supplementary motor area, frontal eye fields, thalamus, and caudate nucleus was related to perceptual consciousness. These data suggest that not all attentional systems are equally effective in enhancing conscious perception, highlighting the importance of thalamo-cortical circuits on the interactions between alerting and consciousness.

Inappropriate rightward saccades after right hemisphere damage: Oculomotor analysis and anatomical correlates.

Patients with right hemisphere damage and visual neglect have severe problems to orient attention towards left-sided objects, often associated with the tendency to produce inappropriate rightward saccades. In its most severe form, this tendency can assume the compulsive character of a rightward deviation of gaze as soon as the visual scene deploys (so-called "magnetic attraction of gaze"). However, little is known about the exact nature of inappropriate rightward saccades, their relation with impaired conscious perception of left-sided stimuli, and their lesional correlates. To explore these issues, we studied three groups of patients with right brain damage: patients with signs of left visual neglect associated to left homonymous hemianopia, neglect patients without hemianopia, and patients without neglect or hemianopia. Participants searched for a gap missing within a target, presented among distractors. Manual responses for target detection were required, while participants were encouraged to move their eyes during search. Endogenous attention could be summoned to the target location by a central cue. All the three groups of patients produced inappropriate rightward saccades, which could not be completely overcome by the endogenous orienting of attention induced by the cues. Anatomical analysis indicated a specific implication of damage to the right frontal eye field and to a long-range white matter tract, the fronto-parietal superior longitudinal fasciculus. Fronto-parietal networks in the right hemisphere appear thus to be essential to integrate covert and overt orienting of attention, and to thoroughly explore space in order to become aware of the multiple competing objects around us.

Subdivision of the occipital lobes: an anatomical and functional MRI connectivity study.

Exploring brain connectivity is fundamental to understanding the functional architecture of the cortex. In our study we employed tractography-based parcellation, combined with the principal component analysis statistical framework, to divide the occipital lobes into seven areas in a group of eighteen healthy participants. Tractography-based parcellation is a method based on diffusion imaging tractography, which segregates the living human brain into distinctive areas showing sharp differences in their anatomical connectivity. The results were compared to covarying functional networks involving distinct areas within the occipital lobes, that we obtained using resting state functional magnetic resonance imaging (fMRI), as well as to other existing subdivisions of the occipital lobes. Our results showed similarities with functional imaging data in healthy controls and cognitive profiles in brain-damaged patients, although several differences with cytoarchitectonic, myelogenetic, myeloarchitectonic and functional maps were reported. While the similarities are encouraging, the potential validity and limitations of the differences observed are discussed. Taken together these results suggest that tractography-based parcellation may provide a new promising anatomical subdivision of the living human brain based on its anatomical connectivity, which may benefit the understanding of clinical-neuroanatomical dissociations and functional neuroimaging results.

Migraine headaches and pain with neuropathic characteristics: comorbid conditions in patients with multiple sclerosis.

We conducted a postal survey to assess the prevalence and characteristics of neuropathic pain and migraine in a cohort of multiple sclerosis (MS) patients. Of the 1300 questionnaires sent, 673 could be used for statistical analysis. Among the respondents, the overall pain prevalence in the previous month was 79%, with 51% experiencing pain with neuropathic characteristics (NCs) and 46% migraine. MS patients with both migraine and NC pain (32% of the respondents) reported more severe pain and had lower health-related quality of life than MS patients with either migraine or NC pain. Pain intensity in MS patients with migraine was moderate (6.0 ± 0.1). Migraine was mostly episodic, but headaches were occurring on ≥15 days per month in 15% of those with migraine. MS patients with migraine were younger and had shorter disease durations than those with NC pain. NC pain was most often located in the extremities, back and head, and was frequently described as tingling and pins-and-needles. The intensity of NC pain was low to moderate (4.9 ± 0.1), but positively correlated with the number of painful body sites. Nonetheless, patients with NC pain were more disabled (with a higher Expanded Disability Status Scale and pain interference index) than patients with migraine. Migraine, but not NC pain, was associated with age, disease duration, relapsing-remitting course, and interferon-beta treatment. This suggests that NC pain and migraine are mediated by different mechanisms. Therefore, pain mechanisms that specifically operate in MS patients need to be characterized to design optimal treatments for these individuals.

Transient suppression of broadband gamma power in the default-mode network is correlated with task complexity and subject performance.

Task performance is associated with increased brain metabolism but also with prominent deactivation in specific brain structures known as the default-mode network (DMN). The role of DMN deactivation remains enigmatic in part because its electrophysiological correlates, temporal dynamics, and link to behavior are poorly understood. Using extensive depth electrode recordings in humans, we provide first electrophysiological evidence for a direct correlation between the dynamics of power decreases in the DMN and individual subject behavior. We found that all DMN areas displayed transient suppressions of broadband gamma (60-140 Hz) power during performance of a visual search task and, critically, we show for the first time that the millisecond range duration and extent of the transient gamma suppressions are correlated with task complexity and subject performance. In addition, trial-by-trial correlations revealed that spatially distributed gamma power increases and decreases formed distinct anticorrelated large-scale networks. Beyond unraveling the electrophysiological basis of DMN dynamics, our results suggest that, rather than indicating a mere switch to a global exteroceptive mode, DMN deactivation encodes the extent and efficiency of our engagement with the external world. Furthermore, our findings reveal a pivotal role for broadband gamma modulations in the interplay between task-positive and task-negative networks mediating efficient goal-directed behavior and facilitate our understanding of the relationship between electrophysiology and neuroimaging studies of intrinsic brain networks.

Emotional facial expression detection in the peripheral visual field.

BACKGROUND: In everyday life, signals of danger, such as aversive facial expressions, usually appear in the peripheral visual field. Although facial expression processing in central vision has been extensively studied, this processing in peripheral vision has been poorly studied. METHODOLOGY/PRINCIPAL FINDINGS: Using behavioral measures, we explored the human ability to detect fear and disgust vs. neutral expressions and compared it to the ability to discriminate between genders at eccentricities up to 40°. Responses were faster for the detection of emotion compared to gender. Emotion was detected from fearful faces up to 40° of eccentricity. CONCLUSIONS: Our results demonstrate the human ability to detect facial expressions presented in the far periphery up to 40° of eccentricity. The increasing advantage of emotion compared to gender processing with increasing eccentricity might reflect a major implication of the magnocellular visual pathway in facial expression processing. This advantage may suggest that emotion detection, relative to gender identification, is less impacted by visual acuity and within-face crowding in the periphery. These results are consistent with specific and automatic processing of danger-related information, which may drive attention to those messages and allow for a fast behavioral reaction.

Unattended emotional faces elicit early lateralized amygdala-frontal and fusiform activations.

Human adaptive behaviour to potential threats involves specialized brain responses allowing rapid and reflexive processing of the sensory input and a more directed processing for later evaluation of the nature of the threat. The amygdalae are known to play a key role in emotion processing. It is suggested that the amygdalae process threat-related information through a fast subcortical route and slower cortical feedback. Evidence from human data supporting this hypothesis is lacking. The present study investigated event-related neural responses during processing of facial emotions in the unattended hemifield using magnetoencephalography (MEG) and found activations of the amygdala and anterior cingulate cortex to fear as early as 100 ms. The right amygdala exhibited temporally dissociated activations to input from different visual fields, suggesting early subcortical versus later cortical processing of fear. We also observed asymmetrical fusiform activity related to lateralized feed-forward processing of the faces in the visual-ventral stream. Results demonstrate fast, automatic, and parallel processing of unattended emotional faces, providing important insights into the specific and dissociated neural pathways in emotion and face perception.

Attention inhibition of early cortical activation to fearful faces.

Several lines of evidence demonstrate that processing facial expression can occur in the first 130 ms following a face presentation, but it remains unclear how this is modulated by attention. We presented neutral, fearful and happy faces to subjects who attended either to repeated identity or to repeated emotions. Brain activity was recorded using magnetoencephalography (MEG) and analyzed with event-related beamforming, providing both temporal and spatial information of processing in the brain. The first MEG component, at 90 ms (M90), was sensitive to facial expression, but only when attention was not directed to expression; non-attended fearful faces increased activation in occipital and right middle frontal gyri. Around 150 ms, activity in several brain regions, regardless of the direction of attention, was larger to emotional compared to neutral faces; attention directed to facial expressions increased activity in the right fusiform gyrus and the anterior insula bilaterally. M220 was not modulated by individual facial expressions; however, attention directed to facial expressions enhanced activity in the right inferior parietal lobe and precuneus, while attention directed to identity enhanced posterior cingulate activity.These data demonstrate that facial expression processing involves frontal brain areas as early as 90 ms. Attention directed to emotional expressions obscured this early automatic processing but increased the M170 activity. The M220 sources varied with the direction of attention. Thus, the pattern of neural activation to faces varied with attention to emotions or to identity, demonstrating separate and only partially overlapping networks for these two facets of information contained in faces.

Unconsciously perceived fear in peripheral vision alerts the limbic system: a MEG study.

BACKGROUND: In ecological situations, threatening stimuli often come out from the peripheral vision. Such aggressive messages must trigger rapid attention to the periphery to allow a fast and adapted motor reaction. Several clues converge to hypothesize that peripheral danger presentation can trigger off a fast arousal network potentially independent of the consciousness spot. METHODOLOGY/PRINCIPAL FINDINGS: In the present MEG study, spatio-temporal dynamics of the neural processing of danger related stimuli were explored as a function of the stimuli position in the visual field. Fearful and neutral faces were briefly presented in the central or peripheral visual field, and were followed by target faces stimuli. An event-related beamformer source analysis model was applied in three time windows following the first face presentations: 80 to 130 ms, 140 to 190 ms, and 210 to 260 ms. The frontal lobe and the right internal temporal lobe part, including the amygdala, reacted as soon as 80 ms of latency to fear occurring in the peripheral vision. For central presentation, fearful faces evoked the classical neuronal activity along the occipito-temporal visual pathway between 140 and 190 ms. CONCLUSIONS: Thus, the high spatio-temporal resolution of MEG allowed disclosing a fast response of a network involving medial temporal and frontal structures in the processing of fear related stimuli occurring unconsciously in the peripheral visual field. Whereas centrally presented stimuli are precisely processed by the ventral occipito-temporal cortex, the related-to-danger stimuli appearing in the peripheral visual field are more efficient to produce a fast automatic alert response possibly conveyed by subcortical structures.