Automatic attention does not equal automatic fear: preferential attention without implicit valence

Theories of nonassociative fear acquisition hold that humans have an innate predisposition for some fears, such as fear of snakes and spiders. This predisposition may be mediated by an evolved fear module (Ohman & Mineka, 2001) that responds to basic perceptual features of threat stimuli by directing attention preferentially and generating an automatic fear response. Visual search and affective priming tasks were used to examine attentional processing and implicit evaluation of snake and spider pictures in participants with different explicit attitudes; controls (n = 25) and snake and spider experts (n = 23). Attentional processing and explicit evaluation were found to diverge; snakes and spiders were preferentially attended to by all participants; however, they were negative only for controls. Implicit evaluations of dangerous and nondangerous snakes and spiders, which have similar perceptual features, differed for expert participants, but not for controls. The authors suggest that although snakes and spiders are preferentially attended to, negative evaluations are not automatically elicited during this processing.     

Of snakes and faces: An evolutionary perspective on the psychology of fear

Snakes and faces are unique stimuli because they are deeply grounded in evolutionarily shaped behavior systems. Snakes are the prototypical stimulus in a predatory defense system promoting escape from predators, which prepares primates for efficient processing, attentional priority, and rapid fear acquisition to snakes and other stimuli related to predation. The social submissiveness system plays a similar role on the social arena by promoting yielding to dominant individuals without jeopardizing the protection of the group. Supporting these theoretical propositions, empirical data from a research program spanning four decades demonstrate enhanced fear conditioning to snakes and threatening faces compared to neutral stimuli, as well as fast nonconscious processing of, and prioritized attention to, snakes and threatening faces. Human brain‐imaging data show that these effects are mediated by an extensive fear‐network centering on the amygdala.     

Right-sided human prefrontal brain activation during acquisition of conditioned fear

This H2(15)O positron emission tomography (PET) study reports on relative regional cerebral blood flow (rCBF) alterations during fear conditioning in humans. In the PET scanner, subjects viewed a TV screen with either visual white noise or snake videotapes displayed alone, then with electric shocks, followed by final presentations of white noise and snakes. Autonomic nervous system responses confirmed fear conditioning only to snakes. To reveal neural activation during acquisition, while equating sensory stimulation, scans during snakes with shocks and white noise alone were contrasted against white noise with shocks and snakes alone. During acquisition, rCBF increased in the right medial frontal gyrus, supporting a role for the prefrontal cortex in fear conditioning to unmasked evolutionary fear-relevant stimuli.     

Snakes and cats in the flower bed: fast detection is not specific to pictures of fear-relevant animals

The observation that snakes and spiders are found faster among flowers and mushrooms than vice versa and that this search advantage is independent of set size supports the notion that fear-relevant stimuli are processed preferentially in a dedicated fear module. Experiment 1 replicated the faster identification of snakes and spiders but also found a set size effect in a blocked, but not in a mixed-trial, sequence. Experiment 2 failed to find faster identification of snake and spider deviants relative to other animals among flowers and mushrooms and provided evidence for a search advantage for pictures of animals, irrespective of their fear relevance. These findings suggest that results from the present visual search task cannot support the notion of preferential processing of fear relevance.     

Selective associations in the observational conditioning of fear in rhesus monkeys

Three experiments explored the issue of selective associations in the observational conditioning of fear. Experiment 1 results indicated that observer rhesus monkeys acquired a fear of snakes through watching videotapes of model monkeys behaving fearfully with snakes. In Experiment 2, observers watched edited videotapes that showed models reacting either fearfully to toy snakes and nonfearfully to artificial flowers (SN+/FL-) or vice versa (FL+/SN-). SN+/FL- observers acquired a fear of snakes but not of flowers; FL+/SN- observers did not acquire a fear of either stimulus. In Experiment 3, monkeys solved complex appetitive discriminative (PAN) problems at comparable rates regardless of whether the discriminative stimuli were the videotaped snake or the flower stimuli used in Experiment 2. Thus, monkeys appear to selectively associate snakes with fear.     

分类和概念对恐惧泛化的影响机制

恐惧泛化与多种焦虑障碍的病理基础密切相关。例如创伤后应激障碍个体往往持续地逃避与创伤事件有关的刺激,遭受着创伤痛苦折磨。本文在厘清知觉辨别与恐惧泛化关系的基础上,着力于高级认知过程(分类与概念相似性、典型性和人工概念)对恐惧泛化的影响,回顾了恐惧泛化的相关神经机制,并揭示恐惧泛化对焦虑障碍患者的临床治疗启示。未来研究应将知觉和高级认知维度的恐惧泛化进行整合研究,同时扩充恐惧习得和泛化的神经回路,以促进人类恐惧泛化更深入的研究。     

Fears, phobias, and preparedness: toward an evolved module of fear and fear learning

An evolved module for fear elicitation and fear learning with 4 characteristics is proposed. (a) The fear module is preferentially activated in aversive contexts by stimuli that are fear relevant in an evolutionary perspective. (b) Its activation to such stimuli is automatic. (c) It is relatively impenetrable to cognitive control. (d) It originates in a dedicated neural circuitry, centered on the amygdala. Evidence supporting these propositions is reviewed from conditioning studies, both in humans and in monkeys; illusory correlation studies; studies using unreportable stimuli; and studies from animal neuroscience. The fear module is assumed to mediate an emotional level of fear learning that is relatively independent and dissociable from cognitive learning of stimulus relationships.     

The lurking snake in the grass: Interference of snake stimuli in visually taxing conditions

Based on evolutionary considerations, it was hypothesized that humans have been shaped to easily spot snakes in visually cluttered scenes that might otherwise hide camouflaged snakes. This hypothesis was tested in a visual search experiment in which I assessed automatic attention capture to evolutionarily-relevant distractor stimuli (snakes), in comparison with another animal which is also feared but where this fear has a disputed evolutionary origin (spiders), and neutral stimuli (mushrooms). Sixty participants were engaged in a task that involved the detection of a target (a bird) among pictures of fruits. Unexpectedly, on some trials, a snake, a spider, or a mushroom replaced one of the fruits. The question of interest was whether the distracting stimuli slowed the reaction times for finding the target (the bird) to different degrees. Perceptual load of the task was manipulated by increments in the set size (6 or 12 items) on different trials. The findings showed that snake stimuli were processed preferentially, particularly under conditions where attentional resources were depleted, which reinforced the role of this evolutionarily-relevant stimulus in accessing the visual system (Isbell, 2009).     

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.     

The influence of animal fear on attentional capture by fear-relevant animal stimuli in children

The present study demonstrated that pictures of fear-relevant animals, snakes and spiders, presented among backgrounds of other animal stimuli captured attention and interfered in the detection of a neutral target to the same extent in a large sample of unselected children (N=81). Moreover, detection of a neutral target animal was slowed more in the presence of a feared fear-relevant distracter, e.g., a snake for snake fearful children, than in the presence of a not feared fear-relevant distracter, e.g., a spider for snake fearful children. These results indicate attentional capture by phylogenetically fear-relevant animal stimuli in children and the selective enhancement of this effect by fear of these animals. These findings are consistent with current models of preferential processing of phylogenetically prepared threat stimuli and with cognitive models of anxiety that propose an enhancing effect of fear in the processing of fear-related stimuli.     

The narrow fellow in the grass: human infants associate snakes and fear

Why are snakes such a common target of fear? One current view is that snake fear is one of several innate fears that emerge spontaneously. Another is that humans have an evolved predisposition to learn to fear snakes. In the first study reported here, 9‐ to 10‐month‐old infants showed no differential spontaneous reaction to films of snakes versus other animals. In the second study, 7‐ to 18‐month‐old infants associated snakes with fear: As predicted, they looked longer at films of snakes while listening to a frightened human voice than while listening to a happy voice. In the third study, infants did not look differentially to still photos of snakes and other animals, indicating that movement is crucial to infants’ association of snakes with fear. These results offer support for the view that humans have a natural tendency to selectively associate snakes with fear.     

The origins of fear of snakes

In the present study, a questionnaire about the nature and origin of fear of snakes was administered to 60 Phobic, 82 Low Fear and 35 High Fear college students. Phobic and High Fear subjects reported greater fear on a variety of components of snake fear. There was little evidence supporting the role of direct conditioning experiences in the acquisition of fear of snakes. Rather, the results suggested a variety of observational and instructional learning experiences as related to the acquisition of snake fear. Although preparedness for direct conditioning does not seem relevant, a preparedness for observational and instructional learning is possible.     

In the grip of fear: Dissociations in attentional processing of animal fearful individuals

Using a modified attention paradigm we investigated specific attentional mechanisms in processing animal feared stimuli. In this paradigm arrays of four pictures were displayed and after its disappearance from view a probe (a letter, X or P) then followed unpredictably in the location of one of the four pictures. The results showed that discriminations of probes tended to be impeded by spider stimuli, compared to snake stimuli. This effect was potentiated by high anxiety but only for those individuals fearful of spiders, since no such effect was observed for snake fearful individuals. Moreover, the discrimination of the probes was not facilitated when presented after the feared stimuli. The implications of these findings are discussed as a function of the cognitive bias involved in specific fear.     

A randomized controlled trial of the effect of D-cycloserine on extinction and fear conditioning in humans

Previous research has shown that D-cycloserine (DCS) facilitates extinction of Pavlovian fear conditioning in rats and enhances exposure therapy in humans. The aim of this study was to test the effect of DCS on extinction of fear conditioning in humans. In three experiments, 238 participants were given either DCS (50 or 500 mg) or placebo 2-3 h before extinction training following a differential shock conditioning paradigm. Clear extinction and recovery (return of fear) effects were observed on both skin conductance and self-reported shock expectancy measures in three studies. DCS had no influence on these effects. The same pattern was observed when the analysis was restricted to aware participants or to good conditioners, when fear-relevant cues (pictures of snakes) were used as the conditioned stimuli, or when analysis was restricted to heightened snake-fearful participants. These results suggest that DCS may not enhance the extinction, or prevent the recovery, of learned fear in a differential Pavlovian conditioning paradigm in humans. Further experimental research is needed to better understand the mechanisms underlying the therapeutic effects of DCS.     

Some animal specific fears are more specific than others: Evidence from attention and emotion measures

Using a visual search methodology we investigated the effect of feared animal stimuli on attention. Our results confirmed the important role of emotion on attention. All participants detected fear-relevant stimuli (snakes and spiders) faster than neutral (mushrooms) ones against a background of fruits. In addition, spider fearful participants were sensitized specifically to detect their feared stimulus (spiders), compared to their fear-relevant but non-feared (snakes) and neutral stimuli. However, for participants fearful of snakes there was no significant difference in detection latencies between the feared (snakes) and the fear-relevant but non-feared animal stimuli (spiders). The results from the attention task were mirrored in the emotional ratings, which showed that spider fear was highly specific, whereas snake fear was associated with a more generalized enhanced evaluation of all negative stimuli.     

Serpent versus surrogate and other determinants of runway fear differences

Avoidance behavior and fear ratings by snake-fearful college volunteers were studied as a function of live vs stuffed snake stimuli, order of presenting the snakes, accompanied (participant modeling format) or unaccompanied social context in the runway test, high or moderate initial fear level and sex of subject. The live snake sponsored more avoidance and rated fear than the specimen, and type of snake stimulus interacted with students' initial fear levels, thus raising questions about previous research using specimens instead of live phobic animal stimuli. Accompanied social context produced generally less fear and avoidance than unaccompanied approach. Numerous complex interactions were found among the type of snake, presentation sequence, social context, sex and fear level variables, raising methodological cautions for future research.     

Fear conditioning and social groups: statistics, not genetics

Humans display more conditioned fear when the conditioned stimulus in a fear conditioning paradigm is a picture of an individual from another race than when it is a picture of an individual from their own race ( Olsson, Ebert, Banaji, & Phelps, 2005 ). These results have been interpreted in terms of a genetic "preparedness" to learn to fear individuals from different social groups ( Ohman, 2005 ; Olsson et al., 2005 ). However, the associability of conditioned stimuli is strongly influenced by prior exposure to those or similar stimuli. Using the Kalman filter, a normative statistical model, this article shows that superior fear conditioning to individuals from other groups is precisely what one would expect if participants perform optimal, Bayesian inference that takes their prior exposures to the different groups into account. There is therefore no need to postulate a genetic preparedness to learn to fear individuals from other races or social groups.     

The detection of fear-relevant stimuli: are guns noticed as quickly as snakes?

Potentially dangerous stimuli are important contenders for the capture of visual-spatial attention, and it has been suggested that an evolved fear module is preferentially activated by stimuli that are fear relevant in a phylogenetic sense (e.g., snakes, spiders, angry faces). In this study, a visual search task was used to test this hypothesis by directly contrasting phylogenetically (snakes) and ontogenetically (guns) fear-relevant stimuli. Results showed that the modern threat was detected as efficiently as the more ancient threat. Thus, both guns and snakes attracted attention more effectively than neutral stimuli (flowers, mushrooms, and toasters). These results support a threat superiority effect but not one that is preferentially accessed by threat-related stimuli of phylogenetic origin. The results are consistent with the view that faster detection of threat in visual search tasks may be more accurately characterized as relevance superiority effects rather than as threat superiority effects.     

Observational conditioning of fear to fear-relevant versus fear-irrelevant stimuli in rhesus monkeys

Two experiments examined whether superior observational conditioning of fear occurs in observer rhesus monkeys that watch model monkeys exhibit an intense fear of fear-relevant, as compared with fear-irrelevant, stimuli. In both experiments, videotapes of model monkeys behaving fearfully were spliced so that it appeared that the models were reacting fearfully either to fear-relevant stimuli (toy snakes or a toy crocodile), or to fear-irrelevant stimuli (flowers or a toy rabbit). Observer groups watched one of four kinds of videotapes for 12 sessions. Results indicated that observers acquired a fear of fear-relevant stimuli (toy snakes and toy crocodile), but not of fear-irrelevant stimuli (flowers and toy rabbit). Implications of the present results for the preparedness theory of phobias are discussed.     

Attentional bias to pictures of fear-relevant animals in a dot probe task

Attentional bias to fear-relevant animals was assessed in 69 participants not preselected on self-reported anxiety with the use of a dot probe task showing pictures of snakes, spiders, mushrooms, and flowers. Probes that replaced the fear-relevant stimuli (snakes and spiders) were found faster than probes that replaced the non-fear-relevant stimuli, indicating an attentional bias in the entire sample. The bias was not correlated with self-reported state or trait anxiety or with general fearfulness. Participants reporting higher levels of spider fear showed an enhanced bias to spiders, but the bias remained significant in low scorers. The bias to snake pictures was not related to snake fear and was significant in high and low scorers. These results indicate preferential processing of fear-relevant stimuli in an unselected sample.