Conserved evolutionary history for quick detection of threatening faces

Humans quickly recognize threats such as snakes and threatening faces, suggesting that human ancestors evolved specialized visual systems to detect biologically relevant threat stimuli. Although non-human primates also detect snakes quickly, it is unclear whether primates share the efficient visual systems to process the threatening faces of their conspecifics. Primates may not necessarily process conspecific threats by facial expressions, because threats from conspecifics in natural situations are often accompanied by other cues such as threatening actions (or attacks) and vocal calls. Here, we show a similar threat superiority effect in both humans and macaque Japanese monkeys. In visual search tasks, monkeys and humans both responded to pictures of a threatening face of an unfamiliar adult male monkey among neutral faces faster than to pictures of a neutral face among threatening faces. However, the monkeys’ response times to detect deviant pictures of a non-face stimulus were not slower when it was shown among threat faces than when it was shown among neutral faces. These results provide the first evidence that monkeys have an attentional bias toward the threatening faces of conspecifics and suggest that threatening faces are evolutionarily relevant fear stimuli. The subcortical visual systems in primates likely process not only snakes, but also more general biological threat-relevant stimuli, including threatening conspecific faces.     

Modulation of auditory spatial attention by visual emotional cues: differential effects of attentional engagement and disengagement for pleasant and unpleasant cues

Previous research has demonstrated that threatening, compared to neutral pictures, can bias attention towards non-emotional auditory targets. Here we investigated which subcomponents of attention contributed to the influence of emotional visual stimuli on auditory spatial attention. Participants indicated the location of an auditory target, after brief (250 ms) presentation of a spatially non-predictive peripheral visual cue. Responses to targets were faster at the location of the preceding visual cue, compared to at the opposite location (cue validity effect). The cue validity effect was larger for targets following pleasant and unpleasant cues compared to neutral cues, for right-sided targets. For unpleasant cues, the crossmodal cue validity effect was driven by delayed attentional disengagement, and for pleasant cues, it was driven by enhanced engagement. We conclude that both pleasant and unpleasant visual cues influence the distribution of attention across modalities and that the associated attentional mechanisms depend on the valence of the visual cue.     

Selective attention to the chemosensory modality

Previous studies have shown that behavioral responses to auditory, visual, and tactile stimuli are modulated by expectancies regarding the likely modality of an upcoming stimulus (see Spence & Driver, 1997). In the present study, we investigated whether people can also selectively attend to the chemosensory modality (involving responses to olfactory, chemical, and painful stimuli). Participants made speeded spatial discrimination responses (left vs. right) to an unpredictable sequence of odor and tactile targets. Odor stimuli were presented to either the left or the right nostril, embedded in a birhinally applied constant airstream. Tactile stimuli were presented to the left or the right hand. On each trial, a symbolic visual cue predicted the likely modality for the upcoming target (the cue was a valid predictor of the target modality on the majority of trials). Response latencies were faster when targets were presented in the expected modality than when they were presented in the unexpected modality, showing for the first time that behavioral responses to chemosensory stimuli can be modulated by selective attention.     

Superior detection of threat-relevant stimuli in infancy

The ability to quickly detect potential threat is an important survival mechanism for humans and other animals. Past research has established that adults have an attentional bias for the detection of threat-relevant stimuli, including snakes and spiders as well as angry human faces. Recent studies have documented that preschool children also detect the presence of threatening stimuli more quickly than various non-threatening stimuli. Here we report the first evidence that this attentional bias is present even in infancy. In two experiments, 8- to 14-month-old infants responded more rapidly to snakes than to flowers and more rapidly to angry than to happy faces. These data provide the first evidence of enhanced visual detection of threat-relevant stimuli in infants and hence offer especially strong support for the existence of a general bias for the detection of threat in humans.     

Switching attention between modalities: further evidence for visual dominance

The present study examined cross-modal selective attention using a task-switching paradigm. In a series of experiments, we presented lateralized visual and auditory stimuli simultaneously and asked participants to make a spatial decision according to either the visual or the auditory stimulus. We observed consistent cross-modal interference in the form of a spatial congruence effect. This effect was asymmetrical, with higher costs when responding to auditory than to visual stimuli. Furthermore, we found stimulus-modality-shift costs, indicating a persisting attentional bias towards the attended stimulus modality. We discuss our findings with respect to visual dominance, directed-attention accounts, and the modality-appropriateness hypothesis.     

Early attention processes and anxiety in children

It has been hypothesized that anxiety in children is associated with attentional bias in the early stages of information processing. Bias towards threat indicates the tendency of an individual to direct attention towards threatening information. The aim of the present study was to investigate whether high test-anxiety in a sample of nonreferred children is associated with attentional bias towards threat pictures, and if low test-anxiety is associated with attentional bias away from threat pictures. A probe-detection task was used with 44 10- to 13-yr.-old children. The overall analyses indicated the presence of an attentional bias away from threatening pictures in these nonreferred children. However, in relation to anxiety, the study did not confirm that high anxious children show an attentional bias towards threatening pictures or that low anxious children show an attentional bias away from threatening pictures. Yet, higher anxiety did seem to be associated with longer mean response times. These longer response times might originate from the interpretation of the nature of a stimulus as too threatening, compared to the actual threatening content, in the first stage of information processing. This finding could be useful to improve treatment methods aimed at anxiety symptoms during childhood.     

Attentional orienting across the sensory modalities

This event-related potential study investigated (i) to what extent incongruence between attention-directing cue and cued target modality affects attentional control processes that bias the system in advance to favor a particular stimulus modality and (ii) to what extent top-down attentional control mechanisms are generalized for the type of information that is to be attended. To this end, both visual and auditory word cues were used to instruct participants to direct attention to a specific visual (color) or auditory (pitch) stimulus feature of a forthcoming multisensory target stimulus. Effects of cue congruency were observed within 200 ms post-cue over frontal scalp regions and related to processes involved in shifting attention from the cue modality to the modality of the task-relevant target feature. Both directing visual attention and directing auditory attention were associated with dorsal posterior positivity, followed by sustained fronto-central negativity. However, this fronto-central negativity appeared to have an earlier onset and was more pronounced when the visual modality was cued. Together the present results suggest that the mechanisms involved in deploying attention are to some extent determined by the modality (visual, auditory) in which attention operates, and in addition, that some of these mechanisms can also be affected by cue congruency.     

Anxiety-related attentional biases and their regulation by attentional control

This study examined the role of self-reported attentional control in regulating attentional biases related to trait anxiety. Simple detection targets were preceded by cues labeling potential target locations as threatening (likely to result in negative feedback) or safe (likely to result in positive feedback). Trait anxious participants showed an early attentional bias favoring the threatening location 250 ms after the cue and a late bias favoring the safe location 500 ms after the cue. The anxiety-related threat bias was moderated by attentional control at the 500-ms delay: Anxious participants with poor attentional control still showed the threat bias, whereas those with good control were better able to shift from the threatening location. Thus, skilled control of voluntary attention may allow anxious persons to limit the impact of threatening information.     

Shared attentional resources for processing visual and chemosensory information

For many years, researchers have argued that we have separate attentional resources for the processing of information impinging on each of our sensory receptor systems. However, a number of recent studies have demonstrated the existence of shared attentional resources for the processing of auditory, visual and tactile stimuli. In the present study, we examined whether there are also common attentional resources for the processing of chemosensory stimuli. Participants made speeded (left vs. right) footpedal discrimination responses to an unpredictable sequence of visual and chemosensory stimuli presented to either nostril. The participants' attention was directed to one or the other modality by means of a symbolic auditory cue (high or low tone) at the start of each trial, which predicted the likely modality for the upcoming target on the majority (80%) of trials. Participants responded more rapidly when the target occurred in the expected modality than when it occurred in the unexpected modality, implying the existence of shared attentional resources for the processing of chemosensory and visual stimuli.     

The time-course of visual threat processing: High trait anxious individuals eventually avert their gaze from angry faces

Several experiments have shown that anxious individuals have an attentional bias towards threat cues. It is also known, however, that exposure to a subjectively threatening but relatively harmless stimulus tends to lead to a reduction in fear. Accordingly, some authors have hypothesised that high trait anxious individuals have a vigilant-avoidant pattern of visual attention to threatening stimuli. In the present study, 52 high trait anxious and 48 low trait anxious subjects were shown pairs of emotional faces, while their direction of gaze was continuously monitored. For 0-1000 ms, both groups were found to view angry faces more than happy faces. For 2000-3000 ms, however, only high trait anxious subjects averted their gaze from angry faces more than they did from happy faces.     

Distracted by danger: Temporal and spatial dynamics of visual selection in the presence of threat

Threatening stimuli are known to influence attentional and visual processes in order to prioritize selection. For example, previous research showed faster detection of threatening relative to nonthreatening stimuli. This has led to the proposal that threatening stimuli are prioritized automatically via a rapid subcortical route. However, in most studies, the threatening stimulus is always to some extent task relevant. Therefore, it is still unclear if threatening stimuli are automatically prioritized by the visual system. We used the additional singleton paradigm with task-irrelevant fear-conditioned distractors (CS+ and CS-) and indexed the time course of eye movement behavior. The results demonstrate automatic prioritization of threat. First, mean latency of saccades directed to the neutral target was increased in the presence of a threatening (CS+) relative to a nonthreatening distractor (CS-), indicating exogenous attentional capture and delayed disengagement of covert attention. Second, more error saccades were directed to the threatening than to the nonthreatening distractor, indicating a modulation of automatically driven saccades. Nevertheless, cumulative distributions of the saccade latencies showed no modulation of threat for the fastest goal-driven saccades, and threat did not affect the latency of the error saccades to the distractors. Together these results suggest that threatening stimuli are automatically prioritized in attentional and visual selection but not via faster processing. Rather, we suggest that prioritization results from an enhanced representation of the threatening stimulus in the oculomotor system, which drives attentional and visual selection. The current findings are interpreted in terms of a neurobiological model of saccade programming.     

Modeling body state-dependent multisensory integration

The brain often integrates multisensory sources of information in a way that is close to the optimal according to Bayesian principles. Since sensory modalities are grounded in different, body-relative frames of reference, multisensory integration requires accurate transformations of information. We have shown experimentally, for example, that a rotating tactile stimulus on the palm of the right hand can influence the judgment of ambiguously rotating visual displays. Most significantly, this influence depended on the palm orientation: when facing upwards, a clockwise rotation on the palm yielded a clockwise visual judgment bias; when facing downwards, the same clockwise rotation yielded a counterclockwise bias. Thus, tactile rotation cues biased visual rotation judgment in a head-centered reference frame. Recently, we have generated a modular, multimodal arm model that is able to mimic aspects of such experiments. The model co-represents the state of an arm in several modalities, including a proprioceptive, joint angle modality as well as head-centered orientation and location modalities. Each modality represents each limb or joint separately. Sensory information from the different modalities is exchanged via local forward and inverse kinematic mappings. Also, re-afferent sensory feedback is anticipated and integrated via Kalman filtering. Information across modalities is integrated probabilistically via Bayesian-based plausibility estimates, continuously maintaining a consistent global arm state estimation. This architecture is thus able to model the described effect of posture-dependent motion cue integration: tactile and proprioceptive sensory information may yield top-down biases on visual processing. Equally, such information may influence top-down visual attention, expecting particular arm-dependent motion patterns. Current research implements such effects on visual processing and attention.     

Modeling body state-dependent multisensory integration

The brain often integrates multisensory sources of information in a way that is close to the optimal according to Bayesian principles. Since sensory modalities are grounded in different, body-relative frames of reference, multisensory integration requires accurate transformations of information. We have shown experimentally, for example, that a rotating tactile stimulus on the palm of the right hand can influence the judgment of ambiguously rotating visual displays. Most significantly, this influence depended on the palm orientation: when facing upwards, a clockwise rotation on the palm yielded a clockwise visual judgment bias; when facing downwards, the same clockwise rotation yielded a counterclockwise bias. Thus, tactile rotation cues biased visual rotation judgment in a head-centered reference frame. Recently, we have generated a modular, multimodal arm model that is able to mimic aspects of such experiments. The model co-represents the state of an arm in several modalities, including a proprioceptive, joint angle modality as well as head-centered orientation and location modalities. Each modality represents each limb or joint separately. Sensory information from the different modalities is exchanged via local forward and inverse kinematic mappings. Also, re-afferent sensory feedback is anticipated and integrated via Kalman filtering. Information across modalities is integrated probabilistically via Bayesian-based plausibility estimates, continuously maintaining a consistent global arm state estimation. This architecture is thus able to model the described effect of posture-dependent motion cue integration: tactile and proprioceptive sensory information may yield top–down biases on visual processing. Equally, such information may influence top–down visual attention, expecting particular arm-dependent motion patterns. Current research implements such effects on visual processing and attention.     

A time-course analysis of attentional cueing by threatening scenes

Models of attention and emotion have assigned a special status to the processing of threatening information: Facilitated attentional capture by threat and its prioritized processing would allow for swift and adequate action to potentially dangerous stimuli. In four experiments, we examined the time-course of facilitated orienting of attention to threatening scenes in the exogenous cueing paradigm. Threat value and presentation duration of the cues were systematically varied. Facilitated attentional capture by threat was limited to highly threatening pictures presented for 100 ms. No attentional effects were observed with a 28 ms cue presentation duration. At slightly longer cue presentations, 200 ms and 500 ms, results indicated no and even reduced attentional capture by threat compared with neutral information. The present results provide support for the idea that threat facilitates fast attentional orienting to its location, followed by the inhibition of attention to threat.     

Attentional biases to threat in social anxiety disorder: time to focus our attention elsewhere?

Background: Cognitive models propose that attentional biases to threat contribute to the maintenance of social anxiety disorder (SAD). However, the specific characteristics of such biases are still object to debate.

Objectives: The current study aimed to disentangle effects of trait and state social anxiety on attention allocation towards social stimuli.

Methods: Participants with SAD (n?=?67) and healthy controls (n?=?62) completed three visual search tasks while their eye movements were recorded. Half of the participants in each group were randomly assigned to a state anxiety induction.

Results: Contrary to our predictions, neither trait nor state social anxiety was associated with a facilitated attention to or a delayed disengagement from threat. However, participants with SAD did show reduced fixation durations for threatening stimuli, indicating an avoidance of threat. Induction of state anxiety led to an increased distractibility by threat.

Conclusions: We suggest that attention allocation in SAD is characterized by an avoidant rather than a vigilant attentional bias. Accordingly, our results contradict previous results that associate SAD with facilitated attention to threat and existing approaches to modify attentional biases, that aim to decrease attention towards threatening stimuli.     

Anxiety and attention to threatening pictures

Previous research using attentional search tasks has revealed an anxiety-related bias favouring attention to threatening words when they are presented simultaneously with emotionally neutral words. In Experiment 1, using a similar task, a related effect was found here with emotionally threatening pictures. When pictures were used as location cues in a second experiment, high-trait anxious individuals were slower than less anxious controls when responding to targets requiring attentional disengagement from threat, and they were slower in general with pictures judged to be highly threatening. In a third experiment using the same task but with a longer cue exposure, a related disengagement difficulty occurred across both groups, although the more general slowing with severe threat was again confined to the anxious group. We conclude that attentional bias involves both a specific difficulty in disengaging attention from the location of any threat and a more general interference effect that is related to threat level.     

The time course of attentional bias to cues of threat and safety

It is well known that relative to neutral stimuli, attention is biased towards processing stimuli that convey threat. In a previous study in which a particular stimulus (e.g. a blue diamond) was associated with the delivery of an electrical shock, the presence of the fear-conditioned stimulus interfered with the execution of voluntary eye movements to other locations. Here, we show that this effect not only occurs early in time, but remains present long after the fear-conditioned stimulus was removed from the screen. In a subsequent experiment, we associated the presence of a particular stimulus with safety, that is, when this stimulus was present it was certain that no electrical shock would be delivered. The presence of the safety signalling stimulus also interfered with the execution of voluntary saccades, but only when the time between stimulus and cue presentation was relatively long. The results indicate that both signals of threat and signals of safety interfere with execution of a saccade long after the source of threat or safety has been removed. However, only threatening stimuli affect saccade execution early in time, suggesting that threatening stimuli drive selection exogenously.     

Investigating the nature and time-course of the modality shift effect between vision and touch

It is well known that stimuli grab attention to their location, but do they also grab attention to their sensory modality? The modality shift effect (MSE), the observation that responding to a stimulus leads to reaction time benefits for subsequent stimuli in the same modality, suggests that this may be the case. If noninformative cue stimuli, which do not require a response, also lead to benefits for their modality, this would suggest that the effect is automatic. We investigated the time-course of the visuotactile MSE and the difference between the effects of cues and targets. In Experiment 1, when visual and tactile tasks and stimulus locations were matched, uninformative cues did not lead to reaction time benefits for targets in the same modality. However, the modality of the previous target led to a significant MSE. Only stimuli that require a response, therefore, appear to lead to reaction time benefits for their modality. In Experiment 2, increasing attention to the cue stimuli attenuated the effect of the previous target, but the cues still did not lead to a MSE. In Experiment 3, a MSE was demonstrated between successive targets, and this effect decreased with increasing intertrial intervals. Overall, these studies demonstrate how cue- and target-induced effects interact and suggest that modalities do not automatically capture attention as locations do; rather, the MSE is more similar to other task repetition effects.     

Investigating the nature and time-course of the modality shift effect between vision and touch

It is well known that stimuli grab attention to their location, but do they also grab attention to their sensory modality? The modality shift effect (MSE), the observation that responding to a stimulus leads to reaction time benefits for subsequent stimuli in the same modality, suggests that this may be the case. If noninformative cue stimuli, which do not require a response, also lead to benefits for their modality, this would suggest that the effect is automatic. We investigated the time-course of the visuotactile MSE and the difference between the effects of cues and targets. In Experiment 1, when visual and tactile tasks and stimulus locations were matched, uninformative cues did not lead to reaction time benefits for targets in the same modality. However, the modality of the previous target led to a significant MSE. Only stimuli that require a response, therefore, appear to lead to reaction time benefits for their modality. In Experiment 2, increasing attention to the cue stimuli attenuated the effect of the previous target, but the cues still did not lead to a MSE. In Experiment 3, a MSE was demonstrated between successive targets, and this effect decreased with increasing intertrial intervals. Overall, these studies demonstrate how cue- and target-induced effects interact and suggest that modalities do not automatically capture attention as locations do; rather, the MSE is more similar to other task repetition effects.     

Threat-based cognitive biases in anxious children: comparison with non-anxious children before and after cognitive behavioural treatment

Attention and interpretation biases for threat stimuli were assessed in 19 anxious (ANX) children before and after cognitive behavioural therapy (CBT), and compared with responses from 19 non-anxious (NA) control children collected over the same period. Attentional bias was assessed using a picture version of the visual probe task with threat, neutral and pleasant pictures. Threat interpretation bias was assessed using both a homographs task in which children used homograph words in a sentence and their neutral or threatening meaning was assessed, and a stories task in which children rated their negative emotion, danger judgments, and influencing ability in ambiguous situations. ANX children showed attention biases towards threat on the visual probe task and threat interpretation biases on the stories task but not the homographs task at pre-treatment in comparison with NA children. Following treatment, ANX children's threat interpretation biases as assessed on the stories task reduced significantly to within levels comparable to NA children. However, ANX children continued to show larger attentional biases towards threat than pleasant pictures on the visual probe task at post-treatment, whereas NA children did not show attentional biases. Moreover, a residual threat interpretation style on the stories task at post-treatment was associated with higher anxiety symptoms in both ANX and NA children.