Sandra C. Soares

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.

Evolutionary derived modulations of attention to two common fear stimuli: Serpents and hostile humans

In this paper we present an evolutionary analysis of attention to stimuli that are threatening from an evolutionary perspective, such as angry faces and snakes. We review data showing that angry, photographically depicted angry faces are more rapidly detected than happy faces in a visual search setting provided that they are male and that distractors are redundant in the sense that they are drawn from a small set of faces. Following Isbells (2009) novel Snake Detection Theory, we predicted that snakes, as the prototypical predators, should be more rapidly detected than spiders, given that spiders have provided less of a predatory threat for primates. We review a series of experiments from our laboratory showing that snakes indeed are more rapidly detected than spiders provided that the target stimuli are presented in a demanding visual context, such as many distractor stimuli, or in peripheral vision. Furthermore, they are more distracting than spiders on the performance of a primary attention task. Because snakes were not affected by perceptual load, whereas spiders followed the usual rule of better detection with low perceptual load, we concluded that attending to snakes might constitute an evolutionary adaptation.

The Distinct Role of the Amygdala, Superior Colliculus and Pulvinar in Processing of Central and Peripheral Snakes.

Introduction Visual processing of ecologically relevant stimuli involves a central bias for stimuli demanding detailed processing (e.g., faces), whereas peripheral object processing is based on coarse identification. Fast detection of animal shapes holding a significant phylogenetic value, such as snakes, may benefit from peripheral vision. The amygdala together with the pulvinar and the superior colliculus are implicated in an ongoing debate regarding their role in automatic and deliberate spatial processing of threat signals. Methods Here we tested twenty healthy participants in an fMRI task, and investigated the role of spatial demands (the main effect of central vs. peripheral vision) in the processing of fear-relevant ecological features. We controlled for stimulus dependence using true or false snakes; snake shapes or snake faces and for task constraints (implicit or explicit). The main idea justifying this double task is that amygdala and superior colliculus are involved in both automatic and controlled processes. Moreover the explicit/implicit instruction in the task with respect to emotion is not necessarily equivalent to explicit vs. implicit in the sense of endogenous vs. exogenous attention, or controlled vs. automatic processes. Results We found that stimulus-driven processing led to increased amygdala responses specifically to true snake shapes presented in the centre or in the peripheral left hemifield (right hemisphere). Importantly, the superior colliculus showed significantly biased and explicit central responses to snake-related stimuli. Moreover, the pulvinar, which also contains foveal representations, also showed strong central responses, extending the results of a recent single cell pulvinar study in monkeys. Similar hemispheric specialization was found across structures: increased amygdala responses occurred to true snake shapes presented to the right hemisphere, with this pattern being closely followed by the superior colliculus and the pulvinar. Conclusion These results show that subcortical structures containing foveal representations such as the amygdala, pulvinar and superior colliculus play distinct roles in the central and peripheral processing of snake shapes. Our findings suggest multiple phylogenetic fingerprints in the responses of subcortical structures to fear-relevant stimuli.

Fear, but not fear-relevance, modulates reaction times in visual search with animal distractors

The research aimed at examining attentional selectivity in a visual search paradigm using pictures of animals that have provided a recurrent threat in an evolutionary perspective (i.e., snakes and spiders) and pictures of animals that have supposedly posed no such threat (i.e., cats and fish). Experiment 1 showed no advantage of fear-relevant stimuli over non-fear-relevant animal stimuli. However, an attentional capture seemed to emerge as a delay in the disengagement of attention, specifically when there was a massive presentation of fear-relevant stimuli in the array. The results from Experiment 2, where participants were selected based specifically on their fear of either snakes or spiders (but not both), showed a preferential processing of the congruent feared stimulus, when compared with non-fearful participants, which strengthens the notion that fear significance may be an important factor drawing attention to a particular spatial location.

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).

The hidden snake in the grass: superior detection of snakes in challenging attentional conditions

Snakes have provided a serious threat to primates throughout evolution. Furthermore, bites by venomous snakes still cause significant morbidity and mortality in tropical regions of the world. According to the Snake Detection Theory (SDT Isbell, 2006; 2009), the vital need to detect camouflaged snakes provided strong evolutionary pressure to develop astute perceptual capacity in animals that were potential targets for snake attacks. We performed a series of behavioral tests that assessed snake detection under conditions that may have been critical for survival. We used spiders as the control stimulus because they are also a common object of phobias and rated negatively by the general population, thus commonly lumped together with snakes as “evolutionary fear-relevant”. Across four experiments (N = 205) we demonstrate an advantage in snake detection, which was particularly obvious under visual conditions known to impede detection of a wide array of common stimuli, for example brief stimulus exposures, stimuli presentation in the visual periphery, and stimuli camouflaged in a cluttered environment. Our results demonstrate a striking independence of snake detection from ecological factors that impede the detection of other stimuli, which suggests that, consistent with the SDT, they reflect a specific biological adaptation. Nonetheless, the empirical tests we report are limited to only one aspect of this rich theory, which integrates findings across a wide array of scientific disciplines.

Exome Analysis Identified a Novel Mutation in the RBP4 Gene in a Consanguineous Pedigree with Retinal Dystrophy and Developmental Abnormalities

Retinitis Pigmentosa (RP) is a common form of retinal degeneration characterized by photoreceptor degeneration and retinal pigment epithelium (RPE) atrophy causing loss of visual field and acuities. Exome sequencing identified a novel homozygous splice site variant (c.111+1G>A) in the gene encoding retinol binding protein 4 (RBP4). This change segregated with early onset, progressive, and severe autosomal recessive retinitis pigmentosa (arRP) in an eight member consanguineous pedigree of European ancestry. Additionally, one patient exhibited developmental abnormalities including patent ductus arteriosus and chorioretinal and iris colobomas. The second patient developed acne from young age and extending into the 5th decade. Both patients had undetectable levels of RBP4 in the serum suggesting that this mutation led to either mRNA or protein instability resulting in a null phenotype. In addition, the patients exhibited severe vitamin A deficiency, and diminished serum retinol levels. Circulating transthyretin levels were normal. This study identifies the RBP4 splice site change as the cause of RP in this pedigree. The presence of developmental abnormalities and severe acne in patients with retinal degeneration may indicate the involvement of genes that regulate vitamin A absorption, transport and metabolism.

Fast detector/first responder : interactions between the superior colliculus-pulvinar pathway and stimuli relevant to primates

Primates are distinguished from other mammals by their heavy reliance on the visual sense, which occurred as a result of natural selection continually favoring those individuals whose visual systems were more responsive to challenges in the natural world. Here we describe two independent but also interrelated visual systems, one cortical and the other subcortical, both of which have been modified and expanded in primates for different functions. Available evidence suggests that while the cortical visual system mainly functions to give primates the ability to assess and adjust to fluid social and ecological environments, the subcortical visual system appears to function as a rapid detector and first responder when time is of the essence, i.e., when survival requires very quick action. We focus here on the subcortical visual system with a review of behavioral and neurophysiological evidence that demonstrates its sensitivity to particular, often emotionally charged, ecological and social stimuli, i.e., snakes and fearful and aggressive facial expressions in conspecifics. We also review the literature on subcortical involvement during another, less emotional, situation that requires rapid detection and response—visually guided reaching and grasping during locomotion—to further emphasize our argument that the subcortical visual system evolved as a rapid detector/first responder, a function that remains in place today. Finally, we argue that investigating deficits in this subcortical system may provide greater understanding of Parkinsons disease and Autism Spectrum disorders (ASD).

A glimpse of fear: Fast detection of threatening targets in visual search with brief stimulus durations

Reliable detection of a threat based on temporally restricted information allows organisms to activate their defensive mechanisms. In the present study we investigated attentional efficiency for prototypical evolutionarily relevant stimuli, snakes (compared with spiders and mushrooms), during visual search conditions in which displays were presented for brief durations and under conditions of high perceptual load. Participants were exposed to a visual search paradigm in which the duration of the display varied between 150 and 300 ms. Perceptual load was manipulated using small, medium, and larger displays (4, 6, and 8 items, respectively). The results showed that fear stimuli, compared with neutral stimuli, were more accurately and quickly detected under both visually degraded conditions. The results also showed differences between the two categories of fear-relevant stimuli (snakes and spiders) in their dependency on perceptual load manipulations. Snake targets were overall detected more accurately than spiders, with this snake advantage effect being more clear-cut with many distracters (high load) than with few (low load). The results were interpreted in light of an evolutionary-based theory (the snake detection theory), which posits that snakes are the prototypical predators of primates.

Nosewitness Identification: Effects of Negative Emotion

Every individual has a unique body odor (BO), similar to a fingerprint. In forensic research, identification of culprit BOs has been performed by trained dogs, but not by humans. We introduce the concept of nosewitness identification and present the first experimental results on BO memory in witness situations involving violent crimes. Two experiments indicated that BO associated with male characters in authentic videos could later be identified in BO lineup tests well above chance. Moreover, culprit BO in emotional crime videos could be identified considerably better than the BO of a male person in neutral videos. This indicates that nosewitness identification benefits from emotional encoding. Altogether, the study testifies to the virtue of body odor as a cue to identify individuals observed under negative emotion.