Generalization of fear is the transfer of the conditioned response (conditioned response, CR) to other similar, but safe stimuli that resemble the original conditioned stimulus (conditioned stimulus, CS; Dunsmoor & Paz, 2015; Jasnow, Lynch, Gilman, & Riccio, 2017; Spalding, 2018). Overgeneralization of fear can be maladaptive, leading individuals to excessive avoidance of safe stimuli, and may also contribute to certain anxiety disorders, such as posttraumatic stress disorder (posttraumatic stress disorder, PTSD) and panic disorder (panic disorder, PD; Ahrens et al., 2016; Hammell, Helwig, Kaczkurkin, Sponheim, & Lissek, 2020; Tinoco-Gonzlez et al., 2015). Given the important role fear generalization plays in psychological trauma, it is necessary to further elucidate this relationship to optimize anxiety-related treatment (Michopoulos, Powers, Gillespie, Ressler, & Jovanovic, 2017; Stegmann et al., 2019).
The classical paradigms of research on anxiety disorders are mainly based on Pavlovian conditioning (Pavlov, 1927). In the classical fear generalization paradigm, a neutral CS (conditioned stimulus, e.g., a 500-Hz tone) is initially paired with an aversive unconditioned stimulus (US; e.g., an electric shock); over time, presenting the CS alone or a generalized stimuli (GS; e.g., a 600-Hz tone) can also come to elicit the CR (e.g., heart rate increasing; Dunsmoor, Kroes, Braren, & Phelps, 2017; Tuominenet et al., 2019). In most previous studies of fear generalization, mild electric shocks (Ahmed & Lovibond, 2015), pictures of snakes or spiders (Dymond, Schlund, Roche, & Whelan, 2014), and loud screams (Ahrens et al., 2016) have been used as traditional aversive US to induce a fear response. The existing question in such paradigms is that the aversive stimulus used as US can often evoke both fear and disgust. Rádlová et al. (2019) demonstrated that snakes are perceived as fearful or disgusting depending on their characteristics, including color, body size, and texture. Further, unpleasant sounds like metal scraping over the slate are alternatives to traditional US used with children and adolescents (Neumann, Waters, & Westbury, 2008). Some people describe the sound of metal scraping as a “chill-sending screech,” because the sounds are sheer torture. It is important to note that very few studies have addressed the confusion between fear and disgust in the conditioning and generalization processes. Some researchers assert that they have used “threatening” or “fear-evoking” stimuli as US; however, the stimulus materials (e.g., International Affective Picture System—IAPS; Lang, Bradley, & Cuthbert, 2008) are, in fact, “negative,” but not necessarily threatening or fear-evoking (Schimmack & Derryberry, 2005). Many aversive IAPS images (International Affective Picture System, which include images “causing strong dislike or disinclination”) representative of salient threats (e.g., images of injuries, mutilations, or burn victims) elicit stronger disgust responses than fear responses (Libkuman, Otani, Kern, Viger, & Novak, 2007).
We approached the current study from the perspective that fear and disgust are two independent, different emotions (Comtesse, & Stemmler, 2017; Klucken et al., 2012). They differ in the display of facial expressions, behavioral responses, physiological responses, and the mechanisms of action and brain activity. Nevertheless, the similarities between fear and disgust make it difficult to disentangle one from the other in terms of emotion elicitation (Rachman, 2004). Specifically, both are unpleasant emotions associated with threat and are often involved in clinical disorders such as obsessive-compulsive disorder (OCD) and agoraphobia. This accounts for a considerable number of studies that have targeted negative emotions in general instead of specific emotions.
OCD is an anxiety disorder characterized by intrusive thoughts, i.e., obsessions (mostly about dirt or germs), and its central symptom is fear of contamination (Armstrong & Olatunji, 2017; Olatunji, Huijding, de Jong, & Smits, 2011; Wood & Tolin, 2002). There is increasing evidence that disgust is the core emotion in OCD (Stein, Liu, Shapira, & Goodman, 2001) associated with repetitive, irrational behavior, such as performing compulsively, the actions of hand washing or cleaning. For example, after putting out the trash, an individual may feel unclean even after excessive hand washing. This shows us how Pavlovian conditioning works, in which a neutral stimulus (hand) becomes an object of disgust after its pairing with the US (trash). Most Pavlovian conditioning research has focused on fear-conditioning, generalization, and extinction; while disgust associative learning studies are limited. Klucken et al. (2012) investigated the neural network underlying fear-conditioned and disgust- conditioned responses using functional magnetic resonance imaging, and revealed that both aversive CRs shared the same ROI-activations, including the cingulate cortex, nucleus accumbens, orbitofrontal cortex, and occipital cortex. In addition, insular activation was found to be sensitive to disgust conditions. Further, compared with fear-associative CS+, disgust-CS + pairing with the disgust stimuli elicits attentional avoidance (Armstrong, McClenahan, Kittle, & Olatunji, 2014). Individuals with blood-injection-injury phobia respond with elevated disgust rather than fear to threat-based US (e.g., blood, injections, and bodily mutilations), suggesting that disgust, but not fear, plays a vital role in the development of blood-injection-injury phobia (Olatunji, Lohr, Smits, Sawchuk, & Patten, 2009). Therefore, it is important to elucidate how individuals differ in response to fear-related and disgust-related associative learning.
The primary aim of the current study was to compare and contrast disgust with fear during Pavlovian associative learning and generalization processes. We expanded prior research by using a novel conditioning paradigm. Participants were exposed to the disgust (or fear) conditioning and generalization task, and the within-subjects design allowed us to disengage the different mechanisms underlying the two threat learning and generalization processes. We measured the US subjective expectation and reaction time in the experimental tasks, and recorded eye movement to capture attentional bias. We hypothesized a greater US expectation for CS + than for CS- in both fear and disgust conditioning phases, and a longer reaction time for fear-related CS than for disgust-related CS. We assumed that fear-related GS1 and GS2 would evoke larger US expectation than would disgust-related GS1 and GS2. Further, we hypothesized pupil enlargement would be greater for fear-related CS+, GS1, and GS2 than for disgust-related stimuli.