Non-social Cues Research Articles

A common and specialized neural code for social attention triggered by eye gaze and biological motion

Humans appear to be endowed with the ability to readily share attention with interactive partners through the utilization of social direction cues, such as eye gaze and biological motion (BM). Here, we investigated the specialized brain mechanism underlying this fundamental social attention ability by incorporating different types of social (i.e., BM, gaze) and non-social (arrow) cues and combining functional magnetic resonance imaging (fMRI) with a modified central cueing paradigm. Using multi-voxel pattern analysis (MVPA), we found that although gaze- and BM-mediated attentional orienting could be decoded from neural activity in a wide range of brain areas, only the right anterior and posterior superior temporal sulcus (aSTS and pSTS) could specifically decode attentional orienting triggered by social but not non-social cues. Critically, cross-category MVPA further revealed that social attention could be decoded across BM and gaze cues in the right STS and the right superior temporal gyrus (STG). However, these regions could not decode attentional orienting across social and non-social cues. These findings together provide evidence for the existence of a specialized social attention module in the human brain, with the right STS/STG being the critical neural site dedicated to social attention.

Mental State Attribution Mediates Exogenous Orienting of Attention Triggered by Gaze Cues, but not Other Social Cues

AbstractWe examined the properties in orienting visual attention that are triggered by social cues (eye gaze or pointing finger) and nonsocial cues (an arrow). Particularly, we investigated whether the mental state of others would be modulated by any social cue. We presented an occluder between the cue and target to manipulate the mental state of an agent in cues (i.e., whether the agent is aware of the target). For Experiment 1, the reaction time (RT) to detect the target was prolonged when the target side was occluded only in the gaze‐cue condition, but not for the arrow or the pointing finger. For Experiment 2, the RT of a discrimination task, which demanded greater cognitive demand, was not prolonged for any cue type. These results suggest that the mental state attribution for the agency of the cue, which is affected by an occluder, is specific to the gaze cue, and suggest that it is under top‐down control that requires cognitive resources.

Visual mental imagery of nonpredictive central social cues triggers automatic attentional orienting

Previous research has demonstrated that social cues (e.g., eye gaze, walking direction of biological motion) can automatically guide people's focus of attention, a well-known phenomenon called social attention. The current research shows that voluntarily generated social cues via visual mental imagery, without being physically presented, can produce robust attentional orienting similar to the classic social attentional orienting effect. Combining a visual imagery task with a dot-probe task, we found that imagining a non-predictive gaze cue could orient attention towards the gazed-at hemifield. Such attentional effect persisted even when the imagery gaze cue was counter-predictive of the target hemifield, and could be generalized to biological motion cue. Besides, this effect could not be simply attributed to low-level motion signal embedded in gaze cues. More importantly, an eye-tracking experiment carefully monitoring potential eye movements demonstrated the imagery-induced attentional orienting effect induced by social cues, but not by non-social cues (i.e., arrows), suggesting that such effect is specialized to visual imagery of social cues. These findings accentuate the demarcation between social and non-social attentional orienting, and may take a preliminary step in conceptualizing voluntary visual imagery as a form of internally directed attention.

Correspondence between the alcohol-P3 event-related potential and alcohol reward phenotypes among young adults.

Behavioral economic theory suggests that the value of alcohol depends upon elements of the choice context, such that increasing constraints on alternatives (e.g., price) or increasing the benefits of alcohol (e.g., social context) may result in greater likelihood of heavy drinking. The P3 event-related potential elicited by alcohol-related cues, a proposed marker of incentive salience, may be an electrophysiological parallel for behavioral economic alcohol demand. However, these indices have not been connected in prior research, and studies typically do not disaggregate social influences in the context of alcohol cue reactivity. The current study recruited heavy drinking young adults (N = 81) who completed measures of alcohol use and alcohol demand, in addition to a 2 (social/nonsocial) × 2 (alcohol/nonalcohol) visual oddball task to elicit the P3. In multilevel models controlling for demographic characteristics, P3 reactivity was greater to alcohol (p < 0.001) and social (p < 0.001) cues than to nonalcohol and nonsocial cues, but without a significant interaction. Higher alcohol consumption (p = 0.02) and lower elasticity of demand (p = 0.01) were associated with greater P3 response to alcohol than nonalcohol cues. The results highlight a brain-behavior connection that may be an important marker for alcohol reward across units of analysis and may be sensitive to changes in the economic choice contexts that influence the likelihood of alcohol use.

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.

Life motion signals bias the perception of apparent motion direction.

Walking direction conveyed by biological motion (BM) cues, which humans are highly sensitive to since birth, can elicit involuntary shifts of attention to enhance the detection of static targets. Here, we demonstrated that such intrinsic sensitivity to walking direction could also modulate the direction perception of simultaneously presented dynamic stimuli. We showed that the perceived direction of apparent motion was biased towards the walking direction even though observers had been informed in advance that the walking direction of BM did not predict the apparent motion direction. In particular, rightward BM cues had an advantage over leftward BM cues in altering the perception of motion direction. Intriguingly, this perceptual bias disappeared when BM cues were shown inverted, or when the critical biological characteristics were removed from the cues. Critically, both the perceptual direction bias and the rightward advantage persisted even when only local BM cues were presented without any global configuration. Furthermore, the rightward advantage was found to be specific to social cues (i.e., BM), as it vanished when non-social cues (i.e., arrows) were utilized. Taken together, these findings support the existence of a specific processing mechanism for life motion signals and shed new light on their influences in a dynamic environment.

Renewal of cocaine seeking using social and nonsocial contextual stimuli.

Various nonsocial cues have been used as stimuli to examine the contextual control of drug seeking behavior, but little is known about the role of social stimuli. This study determined if renewal of cocaine seeking is differentially controlled using a context consisting of either a social peer and/or house light illumination. In Experiment 1, male and female rats trained to self-administer cocaine in the presence of a same-sex social peer and house light illumination (context A). Following self-administration, rats were randomly assigned to either an AAA (control) or ABA (renewal) group for extinction. For AAA rats, extinction consisted of the same context A as self-administration; for ABA rats, extinction occurred without the peer or house light (context B). Following extinction, renewal of cocaine seeking occurred by testing the peer alone, house light alone, and the peer + house light combination. Experiment 2 was conducted to ensure that the house light alone was sufficiently salient to produce renewal. Both experiments showed that rats acquired cocaine self-administration and extinguished lever pressing. In Experiment 1, the ABA group renewed cocaine seeking to the peer and peer + house light, but not to the house light alone. In Experiment 2, ABA rats renewed cocaine seeking to the house light alone, indicating it was sufficiently salient to produce renewal. The AAA group did not show renewal in either experiment. Social peers serve as powerful stimuli that can overshadow nonsocial visual stimuli in the renewal of cocaine seeking.

Deficiency of object-based attention specific to the gaze cue is independent of top-down attentional strategies.

This study investigated whether modes of attentional selection (location-based or object-based) are modulated by the cue type, specifically social cues such as eye gaze and pointing fingers, or by a non-social cue, such as an arrow. Earlier studies have demonstrated that the object-based attention effect was found only with arrow cues when presenting a spatial cue at either end of a rectangle: gaze cues did not yield object-based facilitation. We examined whether this deficiency of object-based attention is generalized to social cues such as pointing fingers. We measured the reaction times to the target at each cued location, an opposite side of a cued location in the same object, or the location in a different object equidistant from the cued location for each cue. Results indicated that only the gaze cue weakened the object-based attention effect, even under the condition of participants' voluntary extension of their attentional focus. The pointing cue induced sufficient object-based facilitation, as did the arrow cue. These results suggest that the deficiency of object-based attention was observed only for the gaze cue, and that it would be caused by a factor that is unique to the gaze cue, which narrows the attentional focus.

Helpers or halos: examining the evaluative mechanisms underlying selective prosociality.

This research examines the proximate evaluative mechanisms underlying prosocial partner choice-based reciprocity. Across four studies we presented 855 university undergraduates (online for course credit) and 76 4- to 6-year-olds (offline at a university laboratory) with vignettes describing prosocial, social and non-social characters, and asked participants about their person preferences in prosocial, social and general contexts. Adults demonstrated sophisticated appraisals, coordinating between relevant trait and contextual cues to make selections. Adults were particularly attentive to prosocial cues in costly conditions, suggesting that they were using dispositional attributions to make their selections. By contrast, children were largely unable to integrate trait and contextual cues in determining their partner preferences, instead displaying valenced preferences for non-social cues, suggesting the use of affective tagging. Together, these studies demonstrate that the mechanisms underlying prosocial, partner choice-based reciprocity are not early emerging and stable but show considerable development over the lifespan.

Exploring the relationship between oculomotor preparation and gaze-cued covert shifts in attention.

Eye gaze plays dual perceptual and social roles in everyday life. Gaze allows us to select information, while also indicating to others where we are attending. There are situations, however, where revealing the locus of our attention is not adaptive, such as when playing competitive sports or confronting an aggressor. It is in these circumstances that covert shifts in attention are assumed to play an essential role. Despite this assumption, few studies have explored the relationship between covert shifts in attention and eye movements within social contexts. In the present study, we explore this relationship using the saccadic dual-task in combination with the gaze-cueing paradigm. Across two experiments, participants prepared an eye movement or fixated centrally. At the same time, spatial attention was cued with a social (gaze) or non-social (arrow) cue. We used an evidence accumulation model to quantify the contributions of both spatial attention and eye movement preparation to performance on a Landolt gap detection task. Importantly, this computational approach allowed us to extract a measure of performance that could unambiguously compare covert and overt orienting in social and non-social cueing tasks for the first time. Our results revealed that covert and overt orienting make separable contributions to perception during gaze-cueing, and that the relationship between these two types of orienting was similar for both social and non-social cueing. Therefore, our results suggest that covert and overt shifts in attention may be mediated by independent underlying mechanisms that are invariant to social context.

Spatial attention to social information in poker: A neuropsychological study using the Posner cueing paradigm.

This research aimed to characterize social information processing abilities in a population of regular nondisordered poker players compared to controls. Participants completed the Posner cueing paradigm task including social cues (faces) to assess attention allocation towards social stimuli, including the effect of the presentation time (subliminal vs supraliminal) and of the emotion displayed. The study included two groups of participants: 30 regular nondisordered poker players (those who played at least three times a week in Texas Hold'em poker games for at least three months) and 30 control participants (those who did not gamble or gambled less than once a month, whatever the game). The group of regular nondisordered poker players displayed anenhancement of the inhibition of return during the Posner cueing task. This means that in valid trials, they took longer to respond to the already processed localization in supraliminal conditions compared to controls. However, our results did not evidence any particular engagement or disengagement attention abilities toward specific types of emotion. These results suggest that regular nondisordered poker players displayed social information processing abilities, which may be due to the importance to efficiently process social information that can serve as tells in live poker. The observed enhancement of the inhibition of return may permit poker players to not process a localization that has already processed to save attentional resources. Further research regarding the establishment of the IOR in other forms of gambling and with non-social cues needs to be performed.

Attention to inattention: effect of the other's attentional state on visual search performance in chimpanzees.

In the present study, we examined the effects of the other's triadic attention to objects on visual search performances in chimpanzees. We found the search-asymmetry-like effect of the other's attentional state; the chimpanzees searched a target object not attended by the other individual more efficiently than that attended (Experiment 1). Additional experiments explored the possibility that the other individual "holding an object but not looking at it" led to expectancy violation (Experiment 2) or the role of nonsocial cues such as the proximity relation between the head and the object (Experiment 3). Still, these accounts alone did not explain this effect. It was also shown that the other's attentional state affected the chimpanzees' performances more readily as the interference effect than the facilitation effect (Experiment 4). Furthermore, the same effect was observed in the visual search for the gaze (head direction) of others (Experiment 5). We obtained the same results using photographs of chimpanzees (Experiment 6). Contrary to the chimpanzees, humans detected the object to which attention was directed more efficiently than vice versa (Experiment 7). The present results may reflect species differences between chimpanzees and humans in processing triadic social attention.

Are you paying attention to me? The effect of social presence on spatial attention to gaze and arrows.

Prior research has shown that the presence of another individual and type of attention cue (social gaze vs. nonsocial arrow) can modulate attention, with little done to integrate the two. We thus investigate the role of two social presence factors when completing a joint cueing task with either social (gaze) or nonsocial (arrow) cues. Familiarity was operationalized as participants engaged in a prompted conversation either before (n = 60 dyads) or after (n = 59 dyads) the task. To determine the effect of previous responder identity on attention, we contrasted trials where participants responded twice in a row (same responder) with switch trials (different responder), along with whether the previous target was in the same or a different location. Although familiarity only affected global speed and not magnitudes of cueing, we did find that attention to gaze and arrows was differentially affected by previous responder and previous target location. Specifically, for gaze cues muted cueing effects occurred for trials where the previous responder was different, while for arrow cues there was less muting of the cueing effect regardless of previous responder. Taken together, previous responder and previous target location both modulated attention, with the effect on attention dependent on the type of cue, gaze, or arrow.

Influences of eye gaze cues on memory and its mechanisms: The function and evolution of social attention.

During evolution, humans have formed a priority perceptual preference for others’ gazes. The gaze direction of others is called the gaze cue, conveying environmental information, a critical non-verbal communication in early humans. Recently, empirical evidence has indicated that gaze cues can affect high-level cognitive processes, such as memory. Unlike non-social cues (e.g., arrows), gaze cues elicit special social attention. Research determining the underlying mechanisms suggests that social intention influences observers’ visual attention and influences their memory. This article provides a brief review of the current state of research on the relationship between gaze cues and memory. Future studies should focus on multiple gaze cues, the social nature of gaze cues, and clinical research.

Internal Social Attention: Gaze Cues Stored in Working Memory Trigger Involuntary Attentional Orienting

Previous research has shown that social cues, including eye gaze, can readily guide our focus of attention—a phenomenon referred to as social attention. Here, we demonstrated that internally maintained social cues in working memory (WM) can produce an analogous attentional effect (N = 57). Using the delayed-match-to-sample paradigm combined with the dot-probe task, we found that holding irrelevant gaze cues in WM can induce attentional orienting in college-age adults. Importantly, this WM-induced attention effect could not be explained simply by the perceptual-attentional process, because the identical gaze cues that were only passively viewed and not memorized in WM could not trigger attentional orienting beyond the typical time window of social attention. Furthermore, nonsocial cues (i.e., arrows) held in WM failed to elicit the attentional-orienting effect. These findings provide new evidence for the conceptualization of WM as internally directed attention and highlight the uniqueness of social attention compared with nonsocial attention.

Does age-related hearing loss deteriorate attentional resources?

ABSTRACT Recent work suggests that age-related hearing loss (HL) is a possible risk factor for cognitive decline in older adults. Resulting poor speech recognition negatively impacts cognitive, social and emotional functioning and may relate to dementia. However, little is known about the consequences of hearing loss on other non-linguistic domains of cognition. The aim of this study was to investigate the role of HL on covert orienting of attention, selective attention and executive control. We compared older adults with and without mild to moderate hearing loss (26–60 dB) performing (1) a spatial cueing task with uninformative central cues (social vs. nonsocial cues), (2) a flanker task and (3) a neuropsychological assessment of attention. The results showed that overall response times and flanker interference effects were comparable across groups. However, in spatial cueing of attention using social and nonsocial cues, hearing impaired individuals were characterized by reduced validity effects, though no additional group differences were found between social and nonsocial cues. Hearing impaired individuals also demonstrated diminished performance on the Montreal Cognitive Assessment (MoCA) and on tasks requiring divided attention and flexibility. This work indicates that while response speed and response inhibition appear to be preserved following mild-to-moderate acquired hearing loss, orienting of attention, divided attention and the ability to flexibly allocate attentional resources are more deteriorated in older adults with HL. This work suggests that hearing loss might exacerbate the detrimental influences of aging on visual attention.

Dopaminergic challenge dissociates learning from primary versus secondary sources of information.

Some theories of human cultural evolution posit that humans have social-specific learning mechanisms that are adaptive specialisations moulded by natural selection to cope with the pressures of group living. However, the existence of neurochemical pathways that are specialised for learning from social information and individual experience is widely debated. Cognitive neuroscientific studies present mixed evidence for social-specific learning mechanisms: some studies find dissociable neural correlates for social and individual learning, whereas others find the same brain areas and, dopamine-mediated, computations involved in both. Here, we demonstrate that, like individual learning, social learning is modulated by the dopamine D2 receptor antagonist haloperidol when social information is the primary learning source, but not when it comprises a secondary, additional element. Two groups (total N = 43) completed a decision-making task which required primary learning, from own experience, and secondary learning from an additional source. For one group, the primary source was social, and secondary was individual; for the other group this was reversed. Haloperidol affected primary learning irrespective of social/individual nature, with no effect on learning from the secondary source. Thus, we illustrate that dopaminergic mechanisms underpinning learning can be dissociated along a primary-secondary but not a social-individual axis. These results resolve conflict in the literature and support an expanding field showing that, rather than being specialised for particular inputs, neurochemical pathways in the human brain can process both social and non-social cues and arbitrate between the two depending upon which cue is primarily relevant for the task at hand.

Atypical processing pattern of gaze cues in dynamic situations in autism spectrum disorders

Psychological studies have generally shown that individuals with Autism Spectrum Disorder (ASD) have particularity in the processing of social information by using static or abstract images. Yet, a recent study showed that there was no difference in their use of social or non-social cues in dynamic interactive situations. To establish the cause of the inconsistent results, we added gaze cues in different directions to the chase detection paradigm to explore whether they would affect the performance of participants with ASD. Meanwhile, eye-tracking methodology was used to investigate whether the processing patterns of gaze cues were different between individuals with ASD and TD. In this study, unlike typical controls, participants with ASD showed no detection advantage when the direction of gaze was consistent with the direction of movement (oriented condition). The results suggested that individuals with ASD may utilize an atypical processing pattern, which makes it difficult for them to use social information contained in oriented gaze cues in dynamic interactive situations.

EEG alpha and theta signatures of socially and non-socially cued working memory in virtual reality.

In this preregistered study (https://osf.io/s4rm9) we investigated the behavioural and neurological [electroencephalography; alpha (attention) and theta (effort)] effects of dynamic non-predictive social and non-social cues on working memory. In a virtual environment realistic human-avatars dynamically looked to the left or right side of a table. A moving stick served as a non-social control cue. Kitchen items were presented in the valid cued or invalid un-cued location for encoding. Behavioural findings showed a similar influence of the cues on working memory performance. Alpha power changes were equivalent for the cues during cueing and encoding, reflecting similar attentional processing. However, theta power changes revealed different patterns for the cues. Theta power increased more strongly for the non-social cue compared to the social cue during initial cueing. Furthermore, while for the non-social cue there was a significantly larger increase in theta power for valid compared to invalid conditions during encoding, this was reversed for the social cue, with a significantly larger increase in theta power for the invalid compared to valid conditions, indicating differences in the cues’ effects on cognitive effort. Therefore, while social and non-social attention cues impact working memory performance in a similar fashion, the underlying neural mechanisms appear to differ.

Social attention triggered by eye gaze and walking direction is resistant to temporal decay.

The attentional orienting induced by social cues, such as eye gaze and walking direction of biological motion, plays a vital role in human survival and interpersonal interactions. It has long been debated whether this indispensable ability is unique and intrinsically distinct from nonsocial attention. In the current study, we characterized the temporal profiles of the attentional orienting triggered by social cues (i.e., eye gaze and walking direction) and compared them with those induced by nonsocial cues (i.e., arrows) and exogenous cues using a covert orienting task. We calculated the attentional cuing effects in the early and the late periods of the task and further carried out a time course analysis to characterize their dynamic changes over trials. Whereas the cuing effect induced by nonsocial cues exhibited a significant trend of temporal decay, the cuing effects induced by the two different social cues were similar and remained stable throughout the task, resembling that induced by reflexive exogenous cues. These results clearly demonstrate that the socially coordinated attentional orienting is a highly reflexive and temporally stable response, which is less susceptible to top-down cognitive control and substantially distinguished from the attentional orienting induced by nonsocial cues. These findings extend our understandings of the distinction between social and nonsocial attention and further substantiate the specificity of social attentional orienting from a temporal-stability perspective. (PsycInfo Database Record (c) 2021 APA, all rights reserved).