Neural basis of social attention: common and distinct mechanisms for social and nonsocial orienting stimuli.

Social and nonsocial directional stimuli (such as gaze and arrows, respectively) share their ability to trigger attentional processes, although the issue of whether social stimuli generate other additional (and unique) attentional effects is still under debate. In this study, we used the spatial interference paradigm to explore, using functional magnetic resonance imaging, shared and dissociable brain activations produced by gaze and arrows. Results showed a common set of regions (right parieto-temporo-occipital) similarly involved in conflict resolution for gaze and arrows stimuli, which showed stronger co-activation for incongruent than congruent trials. The frontal eye field showed stronger functional connectivity with occipital regions for congruent as compared with incongruent trials, and this effect was enhanced for gaze as compared with arrow stimuli in the right hemisphere. Moreover, spatial interference produced by incongruent (as compared with congruent) arrows was associated with increased functional coupling between the right frontal eye field and a set of regions in the left hemisphere. This result was not observed for incongruent (as compared with congruent) gaze stimuli. The right frontal eye field also showed greater coupling with left temporo-occipital regions for those conditions in which larger conflict was observed (arrow incongruent vs. gaze incongruent trials, and gaze congruent vs. arrow congruent trials). These findings support the view that social and nonsocial stimuli share some attentional mechanisms, while at the same time highlighting other differential effects. Highlights Attentional orienting triggered by social (gaze) and nonsocial (arrow) cues is comparable. When social and nonsocial stimuli are used as targets, qualitatively different behavioral effects are observed. This study explores the neural bases of shared and dissociable neural mechanisms for social and nonsocial stimuli. Shared mechanisms were found in the functional coupling between right parieto-temporo-occipital regions. Dissociable mechanisms were found in the functional coupling between right frontal eye field and ipsilateral and contralateral occipito-temporal regions.

Functional characterization of correct and incorrect feature integration.

Our sensory system constantly receives information from the environment and our own body. Despite our impression to the contrary, we remain largely unaware of this information and often cannot report it correctly. Although perceptual processing does not require conscious effort on the part of the observer, it is often complex, giving rise to errors such as incorrect integration of features (illusory conjunctions). In the present study, we use functional magnetic resonance imaging to study the neural bases of feature integration in a dual task that produced ~30% illusions. A distributed set of regions demonstrated increased activity for correct compared to incorrect (illusory) feature integration, with increased functional coupling between occipital and parietal regions. In contrast, incorrect feature integration (illusions) was associated with increased occipital (V1-V2) responses at early stages, reduced functional connectivity between right occipital regions and the frontal eye field at later stages, and an overall decrease in coactivation between occipital and parietal regions. These results underscore the role of parietal regions in feature integration and highlight the relevance of functional occipito-frontal interactions in perceptual processing.

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.

Explicit vs. implicit spatial processing in arrow vs. eye-gaze spatial congruency effects.

Arrows and gaze stimuli lead to opposite spatial congruency effects. While standard congruency effects are observed for arrows (faster responses for congruent conditions), responses are faster when eye-gaze stimuli are presented on the opposite side of the gazed-at location (incongruent trials), leading to a reversed congruency effect (RCE). Here, we explored the effects of implicit vs. explicit processing of arrows and eye-gaze direction. Participants were required to identify the direction (explicit task) or the colour (implicit task) of left or right looking/pointing gaze or arrows, presented to either the left or right of the fixation point. When participants responded to the direction of stimuli, standard congruency effects for arrows and RCE for eye-gaze stimuli were observed. However, when participants responded to the colour of stimuli, no congruency effects were observed. These results suggest that it is necessary to explicitly pay attention to the direction of eye-gaze and arrows for the congruency effect to occur. The same pattern of data was observed when participants responded either manually or verbally, demonstrating that manual motor components are not responsible for the results observed. These findings are not consistent with some hypotheses previously proposed to explain the RCE observed with eye-gaze stimuli and, therefore, call for an alternative plausible hypothesis.

Causal Contributions of the SMA to Alertness and Consciousness Interactions.

Phasic alertness facilitates conscious perception through a fronto-striatal network, including the supplementary motor area (SMA). The functioning of the ventral attentional network has been related to the alerting system, overlapping with the ventral branch of the superior longitudinal fasciculus (SLF III). In this study, we use repetitive transcranial magnetic stimulation (rTMS) and a conscious detection task with near-threshold stimuli that could be preceded by an alerting tone to explore the causal implication of the SMA in the relationship between phasic alertness and conscious perception. Complementary to SMA stimulation, a sham and an active condition (left inferior parietal lobe; IPL) were included. Deterministic tractography was used to isolate the right and left SLF III. Behaviorally, the alerting tone enhanced conscious perception and confidence ratings. rTMS over the SMA reduced the alerting effect on the percentage of perceived stimuli while rTMS over the left IPL produced no modulations, demonstrating a region-specific effect. Additionally, a correlation between the rTMS effect and the integrity of the right SLF III was found. Our results highlight the causal implication of a frontal region, the SMA, in the relationship between phasic alertness and conscious perception, which is related to the white matter microstructure of the SLF III.

Connectivity of Frontoparietal Regions Reveals Executive Attention and Consciousness Interactions.

The executive control network is involved in the voluntary control of novel and complex situations. Solving conflict situations or detecting errors have demonstrated to impair conscious perception of near-threshold stimuli. The aim of this study was to explore the neural mechanisms underlying executive control and its interaction with conscious perception using functional magnetic resonance imaging and diffusion-weighted imaging. To this end, we used a dual-task paradigm involving Stroop and conscious detection tasks with near-threshold stimuli. A set of prefrontal and frontoparietal regions were more strongly engaged for incongruent than congruent trials while a distributed set of frontoparietal regions showed stronger activation for consciously than nonconsciously perceived trials. Functional connectivity analysis revealed an interaction between executive control and conscious perception in frontal and parietal nodes. The microstructural properties of the middle branch of the superior longitudinal fasciculus were associated with neural measures of the interaction between executive control and consciousness. These results demonstrate that conscious perception and executive control share neural resources in frontoparietal networks, as proposed by some influential models.

Target bottom-up strength determines the extent of attentional modulations on conscious perception.

A sufficient level of alerting, bottom-up stimulus strength, and attention have been proposed as important pre-requisites for conscious perception (Dehaene et al. in Trends Cogn Sci 10:204-211, 2006). The combination of different levels of each of these processes might differentially bias the access to consciousness, so that the impact of a specific factor on conscious access would depend on the levels of the other factors. To explore this possibility, we measured how the interaction between different levels of (phasic and tonic) alerting, stimulus bottom-up activation, and endogenous spatial attention, influences conscious perception. We observed that endogenous spatial attention affected conscious perception mainly when target bottom-up strength was low, by improving perceptual sensitivity and making the response criterion stricter. Attention-driven increases of perceptual sensitivity (without variations in response criterion) were also observed for higher levels of bottom-up strength, but only when tonic alerting decreased. Phasic alerting boosted perceptual sensitivity independently of target bottom-up strength, even though it differently affected response bias, yielding a more liberal response criterion when target bottom-up strength increases. These results suggest that a more exhaustive approach to the study of conscious perception should consider the interaction of the multiple factors that are susceptible to modulate perceptual consciousness, rather than studying their effects in isolation.

Causal contributions of the left frontal eye field to conscious perception.

The quest for the neural correlates of consciousness has led to controversial results. When contrasting consciously seen versus unseen stimuli, some authors have proposed that consciousness is related to activity in visual areas along the ventral cortical visual stream, while others propose the implication of parietal and frontal regions ( Dehaene and Changeux 2011). When invisibility is caused by neglect or inattention, high levels of activity recorded in early visual areas ( Vuilleumier et al. 2001) suggest that further activity in fronto-parietal regions might be necessary for conscious perception. Recent functional magnetic resonance imaging evidence ( Chica, Paz-Alonso, et al. 2012) suggested a key role for the left frontal eye field (FEF) in the attentional modulation of visual consciousness. Here, we used the high temporal resolution and causal power of event-related transcranial magnetic stimulation to explore the causal contributions of the left FEF on conscious perception and to assess whether or not these effects are mediated by the orienting of spatial attention. Our results provide the first causal evidence on the contribution of the left FEF to conscious visual perception and indicate that such effects are likely to be mediated by its known role on attentional orienting.

Electrophysiological modulations of exogenous attention by intervening events.

The present study used event related potentials (ERPs) in a spatial cueing procedure to investigate the stages of processing influenced by intervening events presented between cues and targets, when they produce maximal behavioural modulations (i.e., facilitation in the absence of the intervening event, and inhibition of return - IOR, when the intervening event is presented). Our data challenge the traditional orienting-reorienting hypothesis, leading to alternative explanations of cueing effects that are beyond the orienting of attention. Peripheral cues always produced a detection cost (reflected in a reduced amplitude of the P100 component for cued as compared to uncued trials), independently on the behavioural effect that was measured. In contrast, facilitation was associated to modulations of later-stage components, such as N100, Nd, and P300. The N2pc component, usually associated to spatial selection, was the only component reflecting opposite and significant modulations associated to the behavioural effect. The present results suggest that facilitation and IOR can arise from changes at different stages of processing. We propose that the perceptual detection cost (reflected on the P100), and the hindered spatial selection (reflected on the N2pc) at the cued location determine the IOR effect at least in discrimination tasks, while the contribution of the later-stage components, beside attentional processes, determines other facilitatory effects of cueing, which altogether determine the behavioural effect that is measured.

Neural bases of the interactions between spatial attention and conscious perception.

Recent behavioral observations suggest that some forms of attentional orienting have the ability to modulate access to perceptual consciousness. However, the neural structures subserving such processes remain uncertain. We used functional magnetic resonance imaging during a visual discrimination task with near-threshold targets preceded by peripheral cues to identify the neural bases of the interactions between spatial attention and conscious visual perception. During the cue-target period critical for spatial orienting, regions within a frontoparietal network, including nodes of the dorsal attentional system, were more strongly engaged for consciously perceived targets than for nonperceived targets at attended locations. Moreover, activation increased for "unseen" targets in more ventral frontoparietal regions, known to be part of a system involved in attentional reorienting. Functional connectivity analyses revealed tighter coupling between frontoparietal nodes for valid cues leading to "seen" reports and for invalid cues leading to unseen reports. We conclude that spatial orienting to peripheral stimuli, subserved by frontoparietal attentional networks, plays a major role in determining the content of our conscious experience.

When endogenous spatial attention improves conscious perception: effects of alerting and bottom-up activation.

Recent studies have consistently demonstrated that conscious perception interacts with exogenous attentional orienting, but it can be dissociated from endogenous attentional orienting (Chica Lasaponara, et al., 2011; Wyart & Tallon-Baudry, 2008). It has been hypothesized that enhanced conscious processing at exogenously attended locations results from a synergistic action of spatial orienting, bottom-up activation, and phasic alerting induced by the abrupt onset of the exogenous cue (Chica, Lasaponara, et al., 2011). Instead, as endogenous cues need more time to be interpreted, the phasic alerting they produce may have dissipated when the target appears. Furthermore, endogenous cues presumably elicit a weak bottom-up activation at the cued location. Consistent with these hypotheses, we observed that endogenous attention modulated conscious perception, but only when phasic alerting or bottom-up activation was increased. Results are discussed in the context of recent theoretical models of consciousness (Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006).

No support for a causal role of primary motor cortex in construing meaning from language: An rTMS study.

Embodied cognition theories predict a functional involvement of sensorimotor processes in language understanding. In a preregistered experiment, we tested this idea by investigating whether interfering with primary motor cortex (M1) activation can change how people construe meaning from action language. Participants were presented with sentences describing actions (e.g., "turning off the light") and asked to choose between two interpretations of their meaning, one more concrete (e.g., "flipping a switch") and another more abstract (e.g., "going to sleep"). Prior to this task, participants' M1 was disrupted using repetitive transcranial magnetic stimulation (rTMS). The results yielded strong evidence against the idea that M1-rTMS affects meaning construction (BF01 > 30). Additional analyses and control experiments suggest that the absence of effect cannot be accounted for by failure to inhibit M1, lack of construct validity of the task, or lack of power to detect a small effect. In sum, these results do not support a causal role for primary motor cortex in building meaning from action language.

Streams of conscious visual experience.

Consciousness, a cornerstone of human cognition, is believed to arise from complex neural interactions. Traditional views have focused on localized fronto-parietal networks or broader inter-regional dynamics. In our study, we leverage advanced fMRI techniques, including the novel Functionnectome framework, to unravel the intricate relationship between brain circuits and functional activity shaping visual consciousness. Our findings underscore the importance of the superior longitudinal fasciculus within the fronto-parietal fibers, linking conscious perception with spatial neglect. Additionally, our data reveal the critical contribution of the temporo-parietal fibers and the splenium of the corpus callosum in connecting visual information with conscious representation and their verbalization. Central to these networks is the thalamus, posited as a conductor in synchronizing these interactive processes. Contrasting traditional fMRI analyses with the Functionnectome approach, our results emphasize the important explanatory power of interactive mechanisms over localized activations for visual consciousness. This research paves the way for a comprehensive understanding of consciousness, highlighting the complex network of neural connections that lead to awareness.

Integrating brain function and structure in the study of the human attentional networks: a functionnectome study.

Attention is a heterogeneous function theoretically divided into different systems. While functional magnetic resonance imaging (fMRI) has extensively characterized their functioning, the role of white matter in cognitive function has gained recent interest due to diffusion-weighted imaging advancements. However, most evidence relies on correlations between white matter properties and behavioral or cognitive measures. This study used a new method that combines the signal from distant voxels of fMRI images using the probability of structural connection given by high-resolution normative tractography. We analyzed three fMRI datasets with a visual perceptual task and three attentional manipulations: phasic alerting, spatial orienting, and executive attention. The phasic alerting network engaged temporal areas and their communication with frontal and parietal regions, with left hemisphere dominance. The orienting network involved bilateral fronto-parietal and midline regions communicating by association tracts and interhemispheric fibers. The executive attention network engaged a broad set of brain regions and white matter tracts connecting them, with a particular involvement of frontal areas and their connections with the rest of the brain. These results partially confirm and extend previous knowledge on the neural substrates of the attentional system, offering a more comprehensive understanding through the integration of structure and function.

Attention to space and time: Independent or interactive systems? A narrative review.

While there is ample evidence for the ability to selectively attend to where in space and when in time a relevant event might occur, it remains poorly understood whether spatial and temporal attention operate independently or interactively to optimize behavior. To elucidate this important issue, we provide a narrative review of the literature investigating the relationship between the two. The studies were organized based on the attentional manipulation employed (endogenous vs. exogenous) and the type of task (detection vs. discrimination). Although the reviewed findings depict a complex scenario, three aspects appear particularly important in promoting independent or interactive effects of spatial and temporal attention: task demands, attentional manipulation, and their combination. Overall, the present review provides key insights into the relationship between spatial and temporal attention and identifies some critical gaps that need to be addressed by future research.

Impaired attention mechanisms in confabulating patients: A VLSM and DWI study.

Attention is one of the most studied cognitive functions in brain-damaged populations or neurological syndromes, as its malfunction can be related to deficits in other higher cognitive functions. In the present study, we aimed at delimiting the attention deficits of a sample of brain-injured patients presenting confabulations by assessing their performance on alertness, spatial orienting, and executive control tasks. Confabulating patients, who present false memories or beliefs without intention to deceive, usually show memory deficits and/or executive dysfunction. However, it is also likely that attention processes may be impaired in patients showing confabulations. Here, we compared confabulating patients' attention performance to a lesion control group and a healthy control group. Confabulating patients' mean overall accuracy was lower than the one of healthy and lesion controls along the three experimental tasks. Importantly, confabulators presented a greater Simon congruency effect than both lesion controls and healthy controls in the presence of predictive spatial cues, besides a lower percentage of hits and longer RTs in the Go-NoGo task, demonstrating deficits in executive control. They also showed a higher reliance on alerting and spatially predictive orienting cues in the context of a deficient performance. Grey and white matter analyses showed that patients' percentage of hits in the Go-NoGo task was related to damage to the right inferior frontal gyrus (pars triangularis and pars opercularis), whereas the integrity of the right inferior fronto-occipital fasciculus was negatively correlated with their alertness effect. These results are consistent with previous literature highlighting an executive dysfunction in confabulating patients, and suggest that some additional forms of attention, such as alertness and spatial orienting, could be selectively impaired in this clinical syndrome.

A transcranial magnetic stimulation study on the role of the left intraparietal sulcus in temporal orienting of attention.

Adaptive behavior requires the ability to orient attention to the moment in time at which a relevant event is likely to occur. Temporal orienting of attention has been consistently associated with activation of the left intraparietal sulcus (IPS) in prior fMRI studies. However, a direct test of its causal involvement in temporal orienting is still lacking. The present study tackled this issue by transiently perturbing left IPS activity with either online (Experiment 1) or offline (Experiment 2) transcranial magnetic stimulation (TMS). In both experiments, participants performed a temporal orienting task, alternating between blocks in which a temporal cue predicted when a subsequent target would appear and blocks in which a neutral cue provided no information about target timing. In Experiment 1 we used an online TMS protocol, aiming to interfere specifically with cue-related temporal processes, whereas in Experiment 2 we employed an offline protocol whereby participants performed the temporal orienting task before and after receiving TMS. The right IPS and/or the vertex were stimulated as active control regions. While results replicated the canonical pattern of temporal orienting effects on reaction time, with faster responses for temporal than neutral trials, these effects were not modulated by TMS over the left IPS (as compared to the right IPS and/or vertex regions) regardless of the online or offline protocol used. Overall, these findings challenge the causal role of the left IPS in temporal orienting of attention inviting further research on its underlying neural substrates.

Dorsal and ventral parietal contributions to spatial orienting in the human brain.

Influential functional magnetic resonance imaging (fMRI)-based models have involved a dorsal frontoparietal network in the orienting of both endogenous and exogenous attention, and a ventral system in attentional reorienting to task-relevant events. Nonetheless, given the low temporal resolution and susceptibility to epiphenomenal activations of fMRI, such depictions remain highly debated. We hereby benefited from the high temporal resolution and causal power of event-related transcranial magnetic stimulation to explore the implications of key dorsal and ventral parietal regions in those two types of attention. We provide for the first time causal evidence of right intraparietal sulcus involvement in both types of attentional orienting, while we link the temporoparietal junction with the orienting of exogenous but not endogenous spatial attention.

Attention does not always help: The role of expectancy, divided, and spatial attention on illusory conjunctions.

Humans have the subjective impression of a rich perceptual experience, but this perception is riddled with errors that might be produced by top-down expectancies or failures in feature integration. The role of attention in feature integration is still unclear. Some studies support the importance of attention in feature integration, whereas others suggest that feature integration does not require attention. Understanding attention as a heterogeneous system, in this study, we explored the role of divided (as opposed to focused-Experiment 1) attention, and endogenous-exogenous spatial orienting (Experiments 2 and 3) in feature integration. We also explored the role of feature expectancy, by presenting stimulus features that were completely unexpected to the participants. Results demonstrated that both endogenous and exogenous orienting improved feature integration whereas divided attention did not. Moreover, a strong and consistent feature expectancy effect was observed, demonstrating perceptual completion when an unexpected perceptual feature was presented in the scene. These results support the feature confirmation account, which proposes that attention is important for top-down matching of stable representations.

Phasic auditory alerting improves visual conscious perception.

Attention is often conceived as a gateway to consciousness (Posner, 1994). Although endogenous spatial attention may be independent of conscious perception (CP) (Koch Tsuchiya, 2007), exogenous spatial orienting seems instead to be an important modulator of CP (Chica, Lasaponara, Lupiáñez, Doricchi, & Bartolomeo, 2010; Chica, Lasaponara, et al., 2011). Here, we investigate the role of auditory alerting in CP in normal observers. We used a behavioral task in which phasic alerting tones were presented either at unpredictable or at predictable time intervals prior to the occurrence of a near-threshold visual target. We find, for the first time in neurologically intact observers, that phasic alertness increases CP, both objectively and subjectively. This result is consistent with evidence showing that phasic alerting can ameliorate the spatial bias exhibited by visual neglect patients (Robertson, Mattingley, Rorden, & Driver, 1998). The alerting network may increase the activity of fronto-parietal networks involved in top-down amplification required to bring a stimulus into consciousness (Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006).