The preferential detection of threats to survival is an important mechanism in the defensive armoury of any organism placed into a situation where the need for foraging competes with the risk of falling prey to a predator. However, threat detection mechanisms that are highly adaptive at one stage of evolutionary history may become vestigial and even maladaptive at a later one. In primates, the preferential attentional processing of snakes may provide an example for such a development. Snakes are a prime predator of non-human primates to the extent that the selection pressure exerted by snakes shaped the evolutionary development of the primate visual system1 as indicated by the presence of neurons in the medial and dorsolateral pulvinar which show larger and faster responses to images of snakes than to images of threatening conspecifics2. Although snakes pose a lesser threat to the survival of modern humans, fear of snakes remains highly prevalent, even in locations where risk of fatal encounters with snakes is minimal. A large scale Swedish survey, for instance, revealed that 5.5% of a mainly urban sample reported levels of fear of snakes that are clinically relevant and which the respondents described as unjustified, uncontrollable, and impairing their everyday activities3. This rate seems remarkable as there is only one venomous snake native to Sweden (Vipera berus) and fatalities after bites are extremely rare4.

The predisposition to detect and process images of snakes preferentially has been documented in humans and other primates in a number of different paradigms, most prominently in fear conditioning, visual search, and spatial attention tasks5. Fear conditioning is assessed by pairing pictures of snakes or control pictures with aversive outcomes. In humans, preferential fear conditioning to snakes as indexed by physiological responses is evident in that it resists extinction, is selective to aversive learning, can be acquired within a single trial of training, and resists cognitive interventions such as instructions that further unconditional stimuli will not be forthcoming (for reviews see6,7). Similar evidence for preferential learning of a selective association between snakes and negative outcomes has been shown in laboratory reared rhesus monkeys (Macaca mulatta), even in absence of a direct experience of the negative outcome (but6,8, see9 for a qualification).

Visual search has been employed as a paradigm to demonstrate preferential detection of snakes relative to non-threatening stimuli, such as flowers and mushrooms10 or non-threatening animals11. Here, participants are required to detect singleton pictures, e.g., a snake among flowers or a flower among snakes, as quickly as possible. Faster detection of snakes has been shown in human adults and children12 and in Japanese macaques (Macaca fuscata)13,14. Moreover, in human participants the faster detection of snakes is enhanced in participants who self-report high levels of fear of snakes10,15. This observation of individual differences renders it unlikely that preferential detection of snake pictures reflects on low level perceptual features of the stimulus materials used rather than on the content depicted. The evidence from visual search tasks has been criticised, however, as it is not clear whether faster detection of snake than of flower targets reflects on differences in target detection or on slower search through snake than through flower backgrounds11.

A second task that is used, in particular in clinical research, to assess preferential allocation of spatial attention or biased attentional processing is the dot probe task16. In this task, participants are simultaneously presented with two cues, e.g., pictures of a snake and a flower, for a short period of time and after their removal a probe, e.g., a dot, is presented in one of the cued locations. Participants are required to indicate the location or the identity of the probe as quickly as possible. Preferential allocation of attention to one of the images is indicated by faster responding to the probe that replaces this picture, e.g., attentional bias to snakes is evident if the probe replacing the snake is detected faster than the probe replacing the flower, whereas the inverse pattern of results is indicative of avoidance. The dot probe task has been applied to assess attentional bias not only in the context of animal phobias but anxiety disorders more broadly17 and more recently in contexts as diverse as addiction18, obesity and disordered eating19, and pain20. This broad interest reflects on the notion that attentional biases as reflected in the dot probe task may contribute to the development and maintenance of emotional disorders and that their reduction in attentional bias modification training may aid the treatment of these disorders21.

Past research using the dot probe task in human participants has provided evidence that pictures of snakes (or spiders) bias attention and are preferentially attended to and that this bias is larger in participants who reported higher levels of fear of snakes22. Whether a similar attentional bias to snakes in the dot probe task can be observed in non-human primates is currently unclear23. This knowledge gap seems surprising given the importance attributed to attentional biases for the maintenance and mitigation of emotional disorders. Thus, it is important to determine whether such biases can be found in non-human primates or whether they reflect on an evolutionarily relatively recent phenomenon and are limited to Homo sapiens.

While there is no work on attentional bias to snakes in non-human primates, there is some prior work that assesses attentional biases to social stimuli, faces of conspecifics, in macaques. Contrary to predictions, one study failed to find evidence for larger allocation of attention to faces of infants over faces of adults24. However, the remaining two studies reported attentional biases to threatening facial expressions using either faces with neutral expressions25 or scrambled faces26 as controls. Moreover, the former study confirmed that this bias was selective to threatening facial expressions and not evident when positive expressions were presented together with the neutral controls. The prior work on attentional biases in non-human primates confirms the utility of the dot probe paradigm for their assessment. Thus, Experiment 1 will employ the dot probe paradigm to confirm that, like humans, non-human primates (Macaca fuscata) display an attentional bias to snake images.

Although attentional biases in the dot probe task are a well-established phenomenon in humans, it is currently unclear which attentional processes underlie the biases observed24. Faster detection of a probe presented after a picture of a snake may reflect on preferential attentional engagement by snakes, i.e., the faster allocation of attention to snake images. Conversely, it may reflect on a delay of attentional disengagement from snake pictures after attention has been allocated to them. Whereas the former process would suggest a stimulus driven, bottom up attentional process the latter indicates the involvement of top down, goal directed attentional processes. Dissociating these two processes is important not only for a complete understanding of attentional biases, but also for the design of effective interventions as different interventions may differ in their effectiveness to modify them. It should be noted that some of the work on attentional biases in children12 can speak to this dissociation. However, past work in children has largely employed visual search tasks in which it is difficult to differentiate bottom-up and top-down attentional processes11,15.

Koster and colleagues27 suggested the inclusion of baseline trials on which two neutral images, e.g. two images depicting flowers, are presented as a means to dissociate preferential attentional engagement from delayed attentional disengagement in a dot probe task. In brief, preferential engagement is indicated if a probe in the same location as, say, a snake image (snake-valid cued) is found faster than a probe on a baseline trial whereas delayed disengagement is indicated if a probe presented in the location not occupied by the snake (snake-invalid cued) is found slower than a probe on a baseline trial.

Using pictures of mutilations and physical threat scenes, Koster and colleagues found that the attentional bias in their study was mainly driven by delayed disengagement of attention from threat, and a similar pattern emerged in a study that used words as stimulus materials28. However, more recent studies using a modified version of the dot probe task29 or a spatial cuing task30 also provide evidence for preferential attentional engagement by threatening visual stimuli. Experiment 2a will employ a design comprising snake-valid, snake-invalid, and baseline trials to assess whether the attentional bias in Macaca fuscata as shown in Experiment 1 is driven by preferential attentional engagement or delayed attentional disengagement. The study that documented attentional bias to snakes in humans22 did not employ an analysis that would permit the assessment of the underlying attentional processes, but reported performance on snake-valid and snake-invalid cued trials only (as well as spider-valid and spider-invalid cued trials). However, the study included baseline trials in which no animal pictures were presented. Thus, Experiment 2b will report a reanalysis of these data delineating whether the attentional bias to snake images is mediated by the same attentional processes in Homo sapiens and Macaca fuscata.

In summary, the current report is of two experiments conducted in non-human primates and a reanalysis of published data from humans. Experiment 1 was designed to determine whether Japanese macaques (Macaca fuscata) display an attentional bias to pictures of snakes relative to pictures of flowers in a manner similar to that observed in humans22. Experiment 2a included baseline trials on which two flower pictures were shown as cues and was conducted to determine whether attentional bias to snakes in Japanese macaques reflects on preferential attentional engagement to or delayed disengagement from snakes. Experiment 2b reanalysed published data to assess whether the attentional bias in Macaca fuscata and Homo sapiens reflects on the same underlying attentional process.