Differential activation of frontoparietal attention networks by social and symbolic spatial cues.
ABSTRACT: Perception of both gaze-direction and symbolic directional cues (e.g. arrows) orient an observer's attention toward the indicated location. It is unclear, however, whether these similar behavioral effects are examples of the same attentional phenomenon and, therefore, subserved by the same neural substrate. It has been proposed that gaze, given its evolutionary significance, constitutes a 'special' category of spatial cue. As such, it is predicted that the neural systems supporting spatial reorienting will be different for gaze than for non-biological symbols. We tested this prediction using functional magnetic resonance imaging to measure the brain's response during target localization in which laterally presented targets were preceded by uninformative gaze or arrow cues. Reaction times were faster during valid than invalid trials for both arrow and gaze cues. However, differential patterns of activity were evoked in the brain. Trials including invalid rather than valid arrow cues resulted in a stronger hemodynamic response in the ventral attention network. No such difference was seen during trials including valid and invalid gaze cues. This differential engagement of the ventral reorienting network is consistent with the notion that the facilitation of target detection by gaze cues and arrow cues is subserved by different neural substrates.
Project description:The ability to assess another person's direction of attention is paramount in social communication, many studies have reported a similar pattern between gaze and arrow cues in attention orienting. Neuroimaging research has also demonstrated no qualitative differences in attention to gaze and arrow cues. However, these studies were implemented under simple experiment conditions. Researchers have highlighted the importance of contextual processing (i.e., the semantic congruence between cue and target) in attentional orienting, showing that attentional orienting by social gaze or arrow cues could be modulated through contextual processing. Here, we examine the neural activity of attentional orienting by gaze and arrow cues in response to contextual processing using functional magnetic resonance imaging. The results demonstrated that the influence of neural activity through contextual processing to attentional orienting occurred under invalid conditions (when the cue and target were incongruent versus congruent) in the ventral frontoparietal network, although we did not identify any differences in the neural substrates of attentional orienting in contextual processing between gaze and arrow cues. These results support behavioural data of attentional orienting modulated by contextual processing based on the neurocognitive architecture.
Project description:Reorienting of voluntary attention enables the processing of stimuli at previously unattended locations. Although studies have identified a ventral fronto-parietal network underlying attention [1, 2], little is known about whether and how early visual areas are involved in involuntary [3, 4] and even less in voluntary  reorienting, and their temporal dynamics are unknown. We used transcranial magnetic stimulation (TMS) over the occipital cortex to interfere with attentional reorienting and study its role and temporal dynamics in this process. Human observers performed an orientation discrimination task, with either valid or invalid attention cueing, across a range of stimulus contrasts. Valid cueing induced a behavioral response gain increase, higher asymptotic performance for attended than unattended locations. During subsequent TMS sessions, observers performed the same task, with high stimulus contrast. Based on phosphene mapping, TMS double pulses were applied at one of various delays to a consistent brain location in retinotopic areas (V1/V2), corresponding to the evoked signal of the target or distractor, in a valid or invalid trial. Thus, the stimulation was identical for the four experimental conditions (valid/invalid cue condition × target/distractor-stimulated). TMS modulation of the target and distractor were both periodic (5 Hz, theta) and out of phase with respect to each other in invalid trials only, when attention had to be disengaged from the distractor and reoriented to the target location. Reorientation of voluntary attention periodically involves V1/V2 at the theta frequency. These results suggest that TMS probes theta phase-reset by attentional reorienting and help link periodic sampling in time and attention reorienting in space.
Project description:Others' gaze and emotional facial expression are important cues for the process of attention orienting. Here, we investigated with magnetoencephalography (MEG) whether the combination of averted gaze and fearful expression may elicit a selectively early effect of attention orienting on the brain responses to targets. We used the direction of gaze of centrally presented fearful and happy faces as the spatial attention orienting cue in a Posner-like paradigm where the subjects had to detect a target checkerboard presented at gazed-at (valid trials) or non gazed-at (invalid trials) locations of the screen. We showed that the combination of averted gaze and fearful expression resulted in a very early attention orienting effect in the form of additional parietal activity between 55 and 70 ms for the valid versus invalid targets following fearful gaze cues. No such effect was obtained for the targets following happy gaze cues. This early cue-target validity effect selective of fearful gaze cues involved the left superior parietal region and the left lateral middle occipital region. These findings provide the first evidence for an effect of attention orienting induced by fearful gaze in the time range of C1. In doing so, they demonstrate the selective impact of combined gaze and fearful expression cues in the process of attention orienting.
Project description:Three experiments explored attention to eye gaze, which is incompletely understood in typical development and is hypothesized to be disrupted in autism. Experiment 1 (n = 26 typical adults) involved covert orienting to box, arrow, and gaze cues at two probabilities and cue-target times to test whether reorienting for gaze is endogenous, exogenous, or unique; experiment 2 (total n = 80: male and female children and adults) studied age and sex effects on gaze cueing. Gaze cueing appears endogenous and may strengthen in typical development. Experiment 3 tested exogenous, endogenous, and gaze-based orienting in 25 typical and 27 Autistic Spectrum Disorder (ASD) children. ASD children made more saccades, slowing their reaction times; however, exogenous and endogenous orienting, including gaze cueing, appear intact in ASD.
Project description:The right middle fontal gyrus (MFG) has been proposed to be a site of convergence of the dorsal and ventral attention networks, by serving as a circuit-breaker to interrupt ongoing endogenous attentional processes in the dorsal network and reorient attention to an exogenous stimulus. Here, we probed the contribution of the right MFG to both endogenous and exogenous attention by comparing performance on an orientation discrimination task of a patient with a right MFG resection and a group of healthy controls. On endogenously cued trials, participants were shown a central cue that predicted with 90% accuracy the location of a subsequent peri-threshold Gabor patch stimulus. On exogenously cued trials, a cue appeared briefly at one of two peripheral locations, followed by a variable inter-stimulus interval (ISI; range 0-700 ms) and a Gabor patch in the same or opposite location as the cue. Behavioral data showed that for endogenous, and short ISI exogenous trials, valid cues facilitated responses compared to invalid cues, for both the patient and controls. However, at long ISIs, the patient exhibited difficulty in reverting to top-down attentional control, once the facilitatory effect of the exogenous cue had dissipated. When explicitly cued during long ISIs to attend to both stimulus locations, the patient was able to engage successfully in top-down control. This result indicates that the right MFG may play an important role in reorienting attention from exogenous to endogenous attentional control. Resting state fMRI data revealed that the right superior parietal lobule and right orbitofrontal cortex, showed significantly higher correlations with a left MFG seed region (a region tightly coupled with the right MFG in controls) in the patient relative to controls. We hypothesize that this paradoxical increase in cortical coupling represents a compensatory mechanism in the patient to offset the loss of function of the resected tissue in right prefrontal cortex.
Project description:For humans, both eye gaze and arrows serve as powerful signals for orienting attention. Recent studies have shown important differences between gaze and arrows in attention orienting; however, the mechanisms underlying these differences are not known. One such mechanism may be self-referential processing. To investigate this possibility, we trained participants to associate two cues (a red and green arrow in Experiment 1A and two different faces in Experiment 1B) with distinct words ("self" and "other"). Then, we manipulated two types of sound (voice and tone) as targets to investigate whether the cueing effect to self- and other-referential cues differs in a manner similar to that reported for gaze and arrows. We found that self-, but not other-, referential cues induced an enhanced cueing effect to the voice target relative to the tone target regardless of the cue characteristic (i.e., biological or non-biological). Our results suggest that the difference between gaze and arrows in orienting attention can be explained, at least in part, by the self-referentiality of gaze. Furthermore, in Experiment 2, we found a reverse cueing pattern between gaze and arrow cues by manipulating subjects' experiences, suggesting that differences in the self-referentiality of gaze and arrow cues are not inherent.
Project description:Inhibition of return (IOR) is the reduction of detection speed and/or detection accuracy of a target in a recently attended location. This phenomenon, which has been discovered and studied thoroughly in humans, is believed to reflect a brain mechanism for controlling the allocation of spatial attention in a manner that enhances efficient search. Findings showing that IOR is robust, apparent at a very early age and seemingly dependent on midbrain activity suggest that IOR is a universal attentional mechanism in vertebrates. However, studies in non-mammalian species are scarce. To explore this hypothesis comparatively, we tested for IOR in barn owls (Tyto alba) using the classical Posner cueing paradigm. Two barn owls were trained to initiate a trial by fixating on the center of a computer screen and then turning their gaze to the location of a target. A short, non-informative cue appeared before the target, either at a location predicting the target (valid) or a location not predicting the target (invalid). In one barn owl, the response times (RT) to the valid targets compared to the invalid targets shifted from facilitation (lower RTs) to inhibition (higher RTs) when increasing the time lag between the cue and the target. The second owl mostly failed to maintain fixation and responded to the cue before the target onset. However, when including in the analysis only the trials in which the owl maintained fixation, an inhibition in the valid trials could be detected. To search for the neural correlates of IOR, we recorded multiunit responses in the optic tectum (OT) of four head-fixed owls passively viewing a cueing paradigm as in the behavioral experiments. At short cue to target lags (<100?ms), neural responses to the target in the receptive field (RF) were usually enhanced if the cue appeared earlier inside the RF (valid) and were suppressed if the cue appeared earlier outside the RF (invalid). This was reversed at longer lags: neural responses were suppressed in the valid conditions and were unaffected in the invalid conditions. The findings support the notion that IOR is a basic mechanism in the evolution of vertebrate behavior and suggest that the effect appears as a result of the interaction between lateral and forward inhibition in the tectal circuitry.
Project description:Although most studies on social attention have shown undistinguishable attentional effects in response to eye-gaze and arrow cues, recent research has found that whereas the orienting of attention triggered by eye-gaze is directed to the specific position, or part of the object looked at, arrows unselectively elicit attention toward parts of the environment. However, it is unclear whether this dissociation between gaze and arrow cues is related to social cognitive mechanisms such as mental state attribution (Theory of Mind, ToM). We aimed at replicating the dissociation between gaze and arrow cues and investigating if the attentional object selection elicited by these two types of stimuli differs depending on the sex of observers. To make our research plan transparent, our hypotheses, together with the plans of analyses, were registered before data exploration. While we replicated the arrow-gaze dissociation, this was equivalent in the male and female population. These results seem to contradict the intuition that ToM skills can be associated with the differences observed between orienting to eyes and arrows since greater ToM abilities have been generally shown in females. However, this conclusion must be interpreted with caution, since, in our sample, it was not possible to observe any differences in autistic quotient scores and ToM abilities between male and female participants. Further research is needed in order to clarify this issue.
Project description:Eye movements provide important signals for joint attention. However, those eye movements that indicate bids for joint attention often occur among non-communicative eye movements. This study investigated the influence of these non-communicative eye movements on subsequent joint attention responsivity. Participants played an interactive game with an avatar which required both players to search for a visual target on a screen. The player who discovered the target used their eyes to initiate joint attention. We compared participants' saccadic reaction times (SRTs) to the avatar's joint attention bids when they were preceded by non-communicative eye movements that predicted the location of the target (Predictive Search), did not predict the location of the target (Random Search), and when there were no non-communicative eye gaze movements prior to joint attention (No Search). We also included a control condition in which participants completed the same task, but responded to a dynamic arrow stimulus instead of the avatar's eye movements. For both eye and arrow conditions, participants had slower SRTs in Random Search trials than No Search and Predictive Search trials. However, these effects were smaller for eyes than for arrows. These data suggest that joint attention responsivity for eyes is relatively stable to the presence and predictability of spatial information conveyed by non-communicative gaze. Contrastingly, random sequences of dynamic arrows had a much more disruptive impact on subsequent responsivity compared with predictive arrow sequences. This may reflect specialised social mechanisms and expertise for selectively responding to communicative eye gaze cues during dynamic interactions, which is likely facilitated by the integration of ostensive eye contact cues.
Project description:One function of spatial attention is to enable goal-directed interactions with the environment through the allocation of neural resources to motivationally relevant parts of space. Studies have shown that responses are enhanced when spatial attention is predictively biased towards locations where significant events are expected to occur. Previous studies suggest that the ability to bias attention predictively is related to posterior cingulate cortex (PCC) activation [Small, D.M., et al., 2003. The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention. Neuroimage 18, 633-41]. Sleep deprivation (SD) impairs selective attention and reduces PCC activity [Thomas, M., et al., 2000. Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity. J. Sleep Res. 9, 335-352]. Based on these findings, we hypothesized that SD would affect PCC function and alter the ability to predictively allocate spatial attention. Seven healthy, young adults underwent functional magnetic resonance imaging (fMRI) following normal rest and 34-36 h of SD while performing a task in which attention was shifted in response to peripheral targets preceded by spatially informative (valid), misleading (invalid), or uninformative (neutral) cues. When rested, but not when sleep-deprived, subjects responded more quickly to targets that followed valid cues than those after neutral or invalid cues. Brain activity during validly cued trials with a reaction time benefit was compared to activity in trials with no benefit. PCC activation was greater during trials with a reaction time benefit following normal rest. In contrast, following SD, reaction time benefits were associated with activation in the left intraparietal sulcus, a region associated with receptivity to stimuli at unexpected locations. These changes may render sleep-deprived individuals less able to anticipate the locations of upcoming events, and more susceptible to distraction by stimuli at irrelevant locations.