Original Article
Beware the serpent: the advantage of ecologically-relevant stimuli in accessing visual awareness

https://doi.org/10.1016/j.evolhumbehav.2016.10.004Get rights and content

Abstract

Snakes and spiders constitute fear-relevant stimuli for humans, as many species have deleterious and even fatal effects. However, snakes provoked an older and thus stronger evolutionary pressure than spiders, shaping the vision of earliest primates toward preferential visual processing, mainly in the most complex perceptual conditions. To the best of our knowledge, no study has yet directly assessed the role of ecologically-relevant stimuli in preferentially accessing visual awareness. Using continuous flash suppression (CFS), the present study assessed the role of evolutionary pressure in gaining a preferential access to visual awareness. For this purpose, we measured the time needed for three types of stimuli - snakes, spiders (matched with snakes for rated fear levels, but for which an influence on humans but not other primates is well grounded) and birds - to break the suppression and enter visual awareness in two different suppression intensity conditions. The results showed that in the less demanding awareness access condition (stimuli presented to the participants' dominant eye) both evolutionarily relevant stimuli (snakes and spiders) showed a faster entry into visual awareness than birds, whereas in the most demanding awareness access condition (stimuli presented to the participants' non-dominant eye) only snakes showed this privileged access. Our data suggest that the privileged unconscious processing of snakes in the most complex perceptual conditions extends to visual awareness, corroborating the proposed influence of snakes in primate visual evolution.

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

References (107)

  • R.S. Maior et al.

    Superior colliculus lesions impair threat responsiveness in infant capuchin monkeys

    Neuroscience Letters

    (2011)
  • B. Mayer et al.

    Fear-relevant change detection in spider-fearful and non-fearful participants

    Journal of Anxiety Disorders

    (2006)
  • A.D. Milner et al.

    Visual pathways to perception and action

    Progress in Brain Research

    (1993)
  • A.D. Milner et al.

    Two visual systems re-viewed

    Neuropsychologia

    (2008)
  • J.J. New et al.

    Spiders at the cocktail party: An ancestral threat that surmounts inattentional blindness

    Evolution and Human Behavior

    (2015)
  • A. Öhman

    The role of the amygdala in human fear: Automatic detection of threat

    Psychoneuroendocrinology

    (2005)
  • A. Öhman et al.

    On the unconscious subcortical origin of human fear

    Physiology and Behavior

    (2007)
  • B.N. Pasley et al.

    Subcortical discrimination of unperceived objects during binocular rivalry

    Neuron

    (2004)
  • M.J. Penkunas et al.

    Rapid detection of visually provocative animals by preschool children and adults

    Journal of Experimental Child Psychology

    (2013)
  • M.D. Prather et al.

    Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions

    Neuroscience

    (2001)
  • S.C. Soares et al.

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

    Behaviour Research and Therapy

    (2009)
  • T. Stein et al.

    Eye contact facilitates awareness of faces during interocular suppression

    Cognition

    (2011)
  • C. Vakalopoulos

    A theory of blindsight - The anatomy of the unconscious: a proposal for the koniocellular projections and intralaminar thalamus

    Medical Hypotheses

    (2005)
  • J.W. Van Strien et al.

    Snake pictures draw more early attention than spider pictures in non-phobic women: Evidence from event-related brain potentials

    Biological Psychology

    (2014)
  • S. Xu et al.

    Gaze-induced joint attention persists under high perceptual load and does not depend on awareness

    Vision Research

    (2011)
  • J. Almeida et al.

    The role of the dorsal visual processing stream in tool identification

    Psychological Science: A Journal of the American Psychological Society/APS

    (2010)
  • J. Almeida et al.

    Unconscious processing dissociates along categorical lines

    Proceedings of the National Academy of Sciences of the United States of America

    (2008)
  • J. Almeida et al.

    Grasping with the eyes: The role of elongation in visual recognition of manipulable objects

    Cognitive, Affective & Behavioral Neuroscience

    (2014)
  • J. Almeida et al.

    Affect of the unconscious: visually suppressed angry faces modulate our decisions

    Cognitive, Affective & Behavioral Neuroscience

    (2013)
  • I. Almeida et al.

    The distinct role of the amygdala, superior colliculus and pulvinar in processing of central and peripheral snakes

    PloS One

    (2015)
  • I. Arend et al.

    The role of the human pulvinar in visual attention and action: Evidence from temporal-order judgment, saccade decision, and antisaccade tasks

    Progress in Brain Research

    (2008)
  • B. Bahrami et al.

    Unconscious orientation processing depends on perceptual load

    Journal of Vision

    (2008)
  • K. Carlsson et al.

    Fear and the amygdala: Manipulation of awareness generates differential cerebral responses to phobic and fear-relevant (but nonfeared) stimuli

    Emotion (Washington, D.C.)

    (2004)
  • V.A. Casagrande

    A third parallel visual pathway to primate area V1

    Trends in Neurosciences

    (1994)
  • V.A. Casagrande et al.

    Parallel visual pathways: A comparative perspective

  • N.J. Emery et al.

    The role of the amygdala in primate social cognition

  • M.A. Goodale et al.

    Sight unseen: an exploration of conscious and unconscious vision

    (2004)
  • T. Handa et al.

    Effects of dominant and nondominant eyes in binocular rivalry

    Optometry and Vision Science.

    (2004)
  • H. Hongshen et al.

    Spiders do not evoke greater early posterior negativity in the event-related potential as snakes

    Neuroreport

    (2014)
  • L.A. Isbell

    The fruit, the tree, and the serpent

    (2009)
  • M.S. Jensen et al.

    Change blindness and inattentional blindness

    Wiley Interdisciplinary Reviews: Cognitive Science

    (2011)
  • Y. Jiang et al.

    A gender- and sexual orientation-dependent spatial attentional effect of invisible images

    Proceedings of the National Academy of Sciences of the United States of America

    (2006)
  • Y. Jiang et al.

    Processing of invisible stimuli

    Psychological Science : A Journal of the American Psychological Society / APS

    (2007)
  • N.H. Kalin et al.

    The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate

    Journal of Neuroscience

    (2004)
  • A. Kasturiratne et al.

    The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths

    PLoS Medicine

    (2008)
  • L. Kaunitz et al.

    Unseen complex motion is modulated by attention and generates a visible aftereffect

    Journal of Vision

    (2011)
  • L.N. Kaunitz et al.

    Intercepting the first pass: Rapid categorization is suppressed for unseen stimuli

    Frontiers in Psychology

    (2011)
  • H. Kluver et al.

    Preliminary analysis of functions of the temporal lobes in monkeys

    Archives of Neurology & Psychiatry

    (1939)
  • E.I. Knudsen

    Fundamental components of attention

    Annual Review of Neuroscience

    (2007)
  • P.J. Lang et al.

    International affective picture system (IAPS): Technical manual and affective ratings

    NIMH: Center for the Study of emotion and attention

    (1997)
  • Cited by (0)

    View full text