Prepared stimuli enhance aversive learning without weakening the impact of verbal instructions

Abstract

Fear-relevant stimuli such as snakes and spiders are thought to capture attention due to evolutionary significance. Classical conditioning experiments indicate that these stimuli accelerate learning, while instructed extinction experiments suggest they may be less responsive to instructions. We manipulated stimulus type during instructed aversive reversal learning and used quantitative modeling to simultaneously test both hypotheses. Skin conductance reversed immediately upon instruction in both groups. However, fear-relevant stimuli enhanced dynamic learning, as measured by higher learning rates in participants conditioned with images of snakes and spiders. Results are consistent with findings that dissociable neural pathways underlie feedback-driven and instructed aversive learning.[Supplemental material is available for this article.]Human emotion and behavior is influenced by evolutionarily adapted mechanisms that are conserved across organisms. However, humans also learn directly from language and rule-based knowledge. A growing body of research aims to dissociate conserved, biologically prepared processes from those that are sensitive to higher-order influences, such as verbal instruction. The goal of the present study was to test formally how biological preparedness influences aversive learning and its modulation by instructions.Fear-relevant stimuli such as snakes and spiders are thought to engage biologically prepared mechanisms that shape responses and behavior (Seligman 1971;Mineka and Ohman 2002). The extant literature on fear conditioning suggests two main ways in which preparedness can impact conditioning. First, fear-relevant stimuli enhance fear acquisition and retention. Relative to fearirrelevant stimuli (e.g., flowers, mushrooms), fear-relevant stimuli have been shown to facilitate classical conditioning (Ho and Lipp 2014) and slow extinction learning (Fredrikson et al. 1976; Ohman et al. 1975a,b). Work in nonhuman primates suggests that innate responses to fear-relevant stimuli are mediated by the amygdala and orbitofrontal cortex (Meunier et al. 1999;Kalin et al. 2001;Murray and Izquierdo 2007). These structures play crucial roles in fear acquisition (Davis 1992; Maren 2001), extinction (Schiller andDelgado 2010;Milad and Quirk 2012), and value-based learning (Schoenbaum et al. 1998;Holland and Gallagher 2004), and thus their preferential recruitment by prepared stimuli might enhance dynamic aversive learning.Second, a distinct literature indicates that fear-relevant stimuli may be less responsive to instructions about safety. Studies of instructed extinction (Hugdahl and Ohman 1977;Hugdahl 1978) indicate that when individuals are informed that shocks will no longer be delivered following standard Pavlovian conditioning, conditioned responses are abolished immediately in people exposed to neutral stimuli, whereas conditioned responses remain elevated in those conditioned with biologically prepared stimuli. A dominant interpretation of these findings is that fearrelevant stimuli preferentia...

Reversal learning in Drosophila larvae

“…5, 6) and the aversive domain (Figs. 7-9), corresponding to what has been reported for adult flies (Tully and Quinn 1985;Tully et al 1990;Ren et al 2012;Wu et al 2012;Chouhan et al 2015), bees (Giurfa 2003;Mota and Giurfa 2010;Pérez Claudio et al 2018), and vertebrates (Rajalakshmi and Jeeves 1965;O'Malley and Bruning 1969;Morris and Dolan 2004;Bissonette et al 2008;Costa et al 2015;Izquierdo et al 2017;Atlas and Phelps 2018). This suggests reversal learning as a general faculty widespread in the animal kingdom, even where the nervous system is numerically as simple as is the case for the larva with its ∼10,000 neurons (Dumstrei et al 2003;Nassif et al 2003).…”

Facilitating translational science in anxiety disorders by adjusting extinction training in the laboratory to exposure-based therapy procedures

“…The subtle change in the learning context might explain this effect because-in contrast to the day before -no explicit instructions about the contingencies were given. Previous studies have demonstrated that explicit contingency reversal instructions are capable of reversing conditioned responses as measured by SCR [31][32][33][34] , startle reflex 35 , and verbal evaluations 36 . Although contingency reversal was not explicitly modeled, the lack of instruction might have resulted in an ambiguous state of US uncertainty followed by increased physiological responses to both CS+ and CS−.…”

A review on the effects of verbal instructions in human fear conditioning: Empirical findings, theoretical considerations, and future directions

“…Here, participants are informed after a differential conditioning phase that the contingencies from the previous phase will be reversed in the subsequent phase. Research using this procedure has demonstrated that these instructions successfully reversed conditioned SCRs with neutral CSs (Grings et al, 1973;Wilson, 1968) and fear-relevant CSs (i.e., pictures of snakes and spiders) (Atlas & Phelps, 2018;McNally, 1981). Mertens and De Houwer (2016a) have recently extended these studies by demonstrating that also conditioned potentiated startle reflexes can be reversed with contingency reversal instructions.…”

“…Nevertheless, the results of these studies are not uncontested. That is, other studies have demonstrated that verbal instructions can moderate conditioned fear installed via CS-US pairings to fear-relevant CSs as well (Atlas & Phelps, 2018;McNally, 1981;McNally & Foa, 1986; for a review of these studies see McNally, 1987). Likewise, several studies have demonstrated that verbal instructions can abolish differential startle responses established through CS-US pairings (Luck & Lipp, 2015a;2015b;Mertens & De Houwer, 2016a).…”