Introduction

Sensory processing sensitivity (SPS) is proposed to be an innate trait associated with greater sensitivity (or responsivity) to environmental and social stimuli (e.g., Aron et al. 2012). Originally measured in human adults by the Highly Sensitive Person (HSP) scale (Aron and Aron 1997), SPS is becoming increasingly associated with identifiable genes, behavior, physiological reactions, and patterns of brain activation (Aron et al. 2012). A functionally similar trait—termed responsivity, plasticity, or flexibility (Wolf et al. 2008)—has been observed in over 100 nonhuman species including pumpkinseed sunfish (Wilson et al. 1993), birds (Verbeek et al. 1994), rodents (Koolhaas et al. 1999), and rhesus macaques (Suomi 2006).

Sensory processing sensitivity is thought to be one of two strategies that evolved for promoting survival of the species (Aron and Aron 1997; Wolf et al. 2008). By being more responsive to their environments, these more sensitive organisms have an enhanced awareness of opportunities (e.g., food, mates, and alliances) and threats (e.g., predators, loss of status, competitors), and thus may be more ready to respond to emerging situations. This survival strategy is effective as long as the benefits of increased sensitivity outweigh the costs (such as increased cognitive and metabolic demand). In addition to potential costs, those with the sensitive survival strategy will always be in a minority as it would cease to yield special payoffs if it were found in a majority (Wolf et al. 2008).

Humans characterized as high SPS (or HSP) are likely to “pause to check” in novel situations (Aron and Aron 1997; Aron et al. 2012), show heightened awareness of and attention to subtle stimuli, and appear to be more reactive to both positive and negative stimuli (Jagiellowicz 2012). This combination supports a tendency to process stimuli more elaborately and learn from the information gained, which may be useful in the present moment and when applied to future situations. In contrast, those low in SPS pay less attention to subtle stimuli, approach novel situations more quickly, are less emotionally reactive, and behave with less reference to past experiences.

At least two brain imaging studies have examined the attentional and perceptual aspect of SPS in humans, using the HSP scale as a measure of SPS. One study asked individuals to notice subtle differences in photographs of landscapes and found that those with greater SPS showed stronger activation in brain regions for visual and attention processing compared to those low in SPS (Jagiellowicz et al. 2011). A second study, by Aron et al. (2010), compared individuals from East Asia and the United States and showed that SPS moderates the effect of culture on neural responses to culturally relevant cognitive tasks. There was a strong cultural difference in the activation of brain regions associated with attention such that low‐SPS participants showed greater activation when completing tasks that were inconsistent with their cultural context. However, among those high in SPS, there was no cultural difference in brain activation in regions associated with attention. These findings suggest that high‐ (vs. low‐) SPS individuals focus on the task itself independent of other factors.

Studies have also identified genetic polymorphisms' association with SPS. One of these studies (Licht et al. 2011) found an association with polymorphisms of the low‐expressing, short (S) variant of the repeat length polymorphism 5‐HTTLPR (serotonin transporter, 5‐HTT, linked polymorphic region). There is some evidence that carriers of the S‐allele (either two shorts or the short and long combination) are more likely to be depressed in response to stressful life events (Homberg and Lesch 2011). Not surprisingly, since “genetically driven deficient serotonin transporter (5‐HTT) function would not have been maintained throughout evolution if it only exerted negative effects” (Homberg and Lesch 2011, p. 513), increasing research suggests that the S‐allele also has advantages (for a review see Homberg and Lesch 2011). For example, it has been associated with superior performance on perceptual tasks—more risk aversion when there was a low probability of winning, but greater risk seeking when there was a high probability of winning; longer reflection before making difficult choices and better performance on a delayed pattern recognition task (Roiser et al. 2006; Jedema et al. 2009). The role of the S‐allele in a social context has also been studied (e.g., Way and Gurbaxani 2008; Way and Taylor 2010). For example, marital partners with the S‐allele were more affected after a marital discussion by their partner's positive or anxious prediscussion mood (Schoebi et al. 2012). In another study of the possible genetics behind SPS, researchers (Chen et al. 2011) sought to find something closer to the strong associations between genes and traits that are predicted by twin studies but not being found with single gene research. They considered essentially all the genes (98) with polymorphisms that affect the dopamine system, and chose a trait, SPS, “deeply rooted in the nervous system” (p. 1). Employing a multistep approach (ANOVA followed by multiple regression and permutation), they found that 15% of the variance of HSP scale scores were predicted by a set of 10 loci on seven genes.

Evolutionary theories of SPS are still developing and vary (e.g., Wolf et al. 2008, 2011; Ellis et al. 2011; Aron et al. 2012; Pluess and Belsky 2013), but all emphasize that there are advantages to it, many of them being social. For example, responsiveness to others' needs is essential for stabilizing cooperative relationships and trust in humans and other species (e.g., McNamara et al. 2009). Indeed, SPS—whether it is measured by questionnaires, physiological measures, behavioral observations, or genetic markers—confers benefits to individuals in “good‐enough” social environments but vulnerability to negative outcomes in poor ones (e.g., Belsky and Pluess 2009; Pluess and Belsky 2013).

At least two experimental studies relevant to SPS support the idea that it is associated with responsiveness to both positive and negative stimuli. In one experiment, participants were led to believe that they did well or poorly on a general aptitude test (Aron et al. 2005a, Study 4). Those high (vs. low) on SPS had more negative affect when they thought they had low scores on the test, but when they thought they had high scores there was a nonsignificant crossover. In another study, Jagiellowicz (2012) examined the association between SPS (as measured by the HSP scale) and emotional responses to positive and negative images from the International Affective Picture System. High‐ (vs. low‐) SPS individuals rated emotional pictures (especially positive ones) as significantly more positive or negative and tended to respond faster to positives. Also, high‐ versus low‐SPS individuals reporting positive parenting in early childhood reported more arousal to positive pictures. However, the mechanisms by which positive (or negative) social experiences may potentiate the effect of SPS on emotional reactivity have not yet been studied. Moreover, given that SPS is responsive to both positive and negative social environments, we examined whether highly sensitive individuals might show stronger neural responses in predicted brain regions to both positive and negative social stimuli.