Original ArticleBeware the serpent: the advantage of ecologically-relevant stimuli in accessing visual awareness
Introduction
Evolution has equipped humans with a readiness to associate fear with situations that threatened the survival of their ancestors, with potentially deadly predators being a prime example. According to the Snake Detection Theory (SDT; Isbell, 2009) snakes may represent an archetypal fear stimulus. The SDT posits that primates (including humans) have been shaped, by evolutionary arms races, to fear and avoid snakes over evolutionary time (starting about 90–80 million years ago). Isbell, 2006, Isbell, 2009 argues that the selection pressures posed by snakes, as well as the common fear of snakes in humans (Agras, Sylvester, & Oliveau, 1969) and in other primates (Mineka, Keir, & Price, 1980), have favored the origin of primates via changes in the visual system that enabled them to detect and avoid dangerous snakes. Accordingly, several recent studies have provided neurobehavioral evidence for a preferential snake processing in primates. Le et al. (2013), for instance, have shown that neurons in the medial and dorsolateral pulvinar of Japanese monkeys (Macaca fuscata) exhibit faster and stronger responses to snake images (compared with images of faces, hands of monkeys, or simple geometric shapes). In a further study with macaques, Le et al. (2016) found that snakes, again compared with images of faces and hands of monkeys, elicited earlier gamma oscillations (involved in feedforward visual information processing), in macaque pulvinar neurons, confirming that primates can detect snakes very rapidly. Preferential processing of snakes, compared to other stimuli, such as flowers, mushrooms, and other animal stimuli, has also been shown in several visual search tasks in rhesus monkeys (Shibasaki & Kawai, 2009), human children (LoBue and DeLoache, 2008, LoBue et al., 2010, Penkunas and Coss, 2013a, Penkunas and Coss, 2013b, Yorzinski et al., 2014) and human adults (Öhman et al., 2001, Soares and Esteves, 2013, Soares et al., 2014, Soares et al., 2009, Soares, 2012).
This neurobehavioral evidence with humans and monkeys has provided support for the notion that the undeniable need for an effective predatory defense system tailored a fear module – an independent behavioral, psychophysiological and neural system – that is relatively encapsulated from more advanced human cognition in order to foster a successful development of the defense systems (see Öhman & Mineka, 2001). Although there is evidence that the fear module is selectively sensitive and automatically activated by evolutionary-relevant fear stimuli, the results from most of these studies preclude a direct test of the SDT, since no equivalent animal fear stimuli with distinct evolutionary baggage have been considered for comparison. More recently, however, Soares and her colleagues (Soares, 2012, Soares et al., 2009, Soares and Esteves, 2013, Soares et al., 2014) proposed spiders as the ideal candidate for humans, based on the premise, derived from the SDT, that selection has favored perceptual abilities to detect snakes more strongly than spiders (Isbell, 2009). Spiders attack other spiders and insects (Nyffeler, 1999) and, unlike poisonous snakes, spiders' poison did not evolve to be effective against mammals (Gerdes, Uhl, & Alpers, 2009). Moreover, unlike snakes, that continue to pose a threat to human life even today (Kasturiratne et al., 2008), only a small amount of spiders have a direct contact with humans and only a few are considered as a cause of morbidity or mortality (e.g., Steen, Carbonaro, & Schwartz, 2004). Hence, the perceptual abilities to detect camouflaged snakes have been more consistently selected for among serpents than among arachnids, making the genes promoting defense against snakes more prominent among the former than the latter (Isbell, 2009). Therefore, spiders are the ideal comparison stimuli to test the SDT, because they are also fear-relevant for humans, compared to snakes, but have a distinct evolutionary baggage. Moreover, snake and spider stimuli are matched for fear levels in humans (Lang, Bradley, & Cuthbert, 2005) and are both highly frequent objects of phobias (e.g., Agras et al., 1969). Following this premise, a growing body of behavioral (e.g., faster detection in visual search settings) and electrophysiological data (maximal amplitudes in specific early attention-related brain potentials; P1 and EPN) has now provided more direct evidence in favor of snakes' preferential processing, compared to spiders and innocuous animal stimuli (other reptiles, insects, birds, and slugs) (Hongshen et al., 2014, Soares et al., n.d, Van Strien et al., 2014a, Van Strien et al., 2014b). More importantly, and conforming to the predictions of the SDT (Isbell, 2009), snake preferential processing has been observed particularly under conditions that may have been critical for survival, such as those involved in taxing visual conditions, such as peripheral visual field (Soares, Lindström, Esteves and Öhman, 2014), brief exposure durations (Soares and Esteves, 2013, Soares et al., 2014), and a more cluttered environment (Soares, 2012, Soares and Esteves, 2013, Soares et al., 2009, Soares et al., 2014).
As proposed by Öhman and Mineka (2001), the rapid and efficient processing of evolutionary-relevant stimuli by the fear module may occur without the need for conscious processing before a response is elicited, most likely due to a dedicated neural circuitry, centered in the amygdala, that bypasses the visual cortex (e.g., Phelps & LeDoux, 2005; but see Pessoa & Adolphs, 2010). Although some studies have shown that such stimuli are processed preferentially outside of awareness, researchers were targeting the neurobehavioral responses of phobic participants, with no interest in showing dissociations between snake and spider stimuli (Carlsson et al., 2004, Öhman and Soares, 1994). Moreover, the authors have mainly used the backward masking (BM) paradigm to render the stimuli under unconscious awareness for a limited time frame (<40 ms) (see Wiens, 2006), and without examining whether the fear stimuli hold an advantage in entering into visual awareness.
Recently, interest in how emotional (fear) stimuli are processed under unawareness has grown, partly due to the emergence of interocular suppression techniques, such as the continuous flash suppression (CFS; Tsuchiya & Koch, 2005). This technique allows stronger and more time enduring states of unawareness (around ten times longer than BM) due to the suppression of static images by dynamic noise. Several studies have demonstrated that threatening stimuli, such as fearful faces (Stein et al., 2014, Sterzer et al., 2011, Tsuchiya et al., 2009, Yang et al., 2007), faces with a direct gaze (Stein, Senju, Peelen, & Sterzer, 2011), angry body postures (Zhan, Hortensius, & De Gelder, 2015), and spiders (Schmack, Burk, Haynes, & Sterzer, 2015), emerge faster into awareness (breaking-CFS; Jiang, Costello, & He, 2007) than neutral stimuli. In this context, it is worth noting that these previous studies with CFS showing that threat-related stimuli gain a preferential access to visual awareness, have mostly considered social stimuli, i.e., differences in facial expression and bodily posture. However, as we have discussed above, ecological stimuli are also important. To the best of our knowledge no study has yet directly investigated the role of ecologically relevant fear stimuli in accessing awareness, comparing stimuli with and without such relevance. Although Schmack et al. (2015) have used spiders, the authors were only interested in studying the phobic characteristics of the stimulus, thus not attending to their evolutionary relevance. Accordingly, studies using other methodologies aiming at testing the access to visual awareness, such as change blindness and intentional blindness (for a review see Jensen, Yao, Street, & Simons, 2011), have evidenced that spiders are detected, located, and identified by a higher percentage of observers, both by participants with a specific phobia to the stimulus (Peira, Golkar, Larsson, & Wiens, 2010), and by participants with no such phobia (Mayer et al., 2006, New and German, 2015;). However, and as in the study by Schmack et al. (2015), none of these studies were interested in studying the role of the evolutionary relevance of the stimulus in entering visual awareness.
In the present study, we used CFS to investigate whether snakes overcame suppression and entered into awareness faster than spiders (compared to birds, an innocuous animal stimulus) in humans. Based on previous results showing preferential processing of evolutionarily relevant stimuli by the fear module, the first prediction of this study was that both snakes and spiders (when compared with birds) would have an advantage in entering into visual awareness (reflected in faster reaction times, RTs). Furthermore, and since no study has yet directly investigated the role of ecological stimuli in gaining preferential access to visual awareness, as mentioned earlier, we directly compared two stimuli with distinctly different evolutionary relevance for primates - snakes and spiders. Inspired by the SDT, (Isbell, 2009) and based on previous findings showing a facilitated processing of snakes (compared to spiders and neutral stimulus) under the most perceptually demanding conditions (e.g., Soares, Lindström, Esteves and Öhman, 2014) we considered, as our second prediction, that snakes would have an advantage in entering into awareness (reflected in faster RTs), compared to spiders (and innocuous animals, birds) in the most complex perceptual condition. In order to create two distinct perceptual complexity conditions during CFS, we divided participants based on their ocular dominance. The concept of ocular dominance (see Porac & Coren, 1976) refers to an evident monocular processing preference when the images viewed by the two eyes cannot be merged, such as in a dichotic stimulation condition (Valle-Inclán, Blanco, Soto, & Leirós, 2008). Data from studies that use binocular rivalry paradigms (also an interocular suppression technique) have shown that a stimulus presented to the dominant eye (assessed with sight dominance tests, such as Miles' test; see Miles, 1930) was visible for longer periods and was detected with higher accuracy than a stimulus presented to the non-dominant eye (e.g., Handa et al., 2004, Valle-Inclán et al., 2008). These data suggest a preference for processing stimuli when these are presented to the dominant eye over stimuli presented to the non-dominant eye. Therefore, during CFS, presenting the stimulus to the dominant eye or to the non-dominant eye of the participant may represent different conditions of suppression, with the latter being a more demanding stimulus detection condition. Thus, we predict that snakes will have an advantage in entering into visual awareness (reflected in faster RTs) in the most demanding suppression condition (i.e., when stimuli are presented to the non-dominant eye) compared to spiders, for which evolutionary pressures were weaker (and innocuous animals, birds) (see Soares, Lindström, Esteves and Öhman, 2014). However, in the less demanding suppression condition (i.e., when stimuli are presented to the dominant eye), although we expect both snakes and spiders to have an advantage in entering into awareness (when compared with birds), no differences are expected between the two, as they are both fear-relevant stimuli for humans (e.g., Agras et al., 1969).
Section snippets
Participants
Sixty-one university students (forty-six women), aged between 17 and 42 (M = 21.64, SD = 4.16), participated voluntarily in the experiment after informed consent. Participants were screened for ocular dominance, revealing 32 participants with right dominance (23 women), aged 18 to 35 (M = 22.03; SD = 3.90), and 29 participants with left dominance (22 women), aged 17 to 42 (M = 21.21, SD = 4.45). All participants reported normal, or corrected to normal eyesight, no psychiatric medication intake, and no
Results
Conforming to our first prediction, the results showed a significant main effect of animal stimuli [F(2, 118) = 24.43, p < 0.001, η2p = 0.29], with snakes and spiders (M = 3927.50 ms; SD = 982.70, and M = 3918.58 ms; SD = 1022.98, respectively) showing faster access to visual awareness than birds (M = 4099.46 ms; SD = 1006.65), as confirmed by Bonferroni post-hoc comparisons (p < 0.001). No statistically significant differences were found between snakes and spiders (p = 1.000).
The results also showed a significant
Discussion
In the present study we assessed the average reaction times for snakes and spiders (stimuli with different histories as dangerous stimuli to primates) in entering into awareness (compared to an innocuous animal stimulus, birds), across two different suppression conditions. Confirming our first prediction, the results showed an advantage of emotional stimuli in general (snakes and spiders vs birds), corroborating the evidence that emotional stimuli (e.g., fearful faces) gain preferential access
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