Abstract

Money is a secondary reinforcer commonly used across a range of disciplines in experimental paradigms investigating reward learning and decision-making. The effectiveness of monetary reinforcers during aversive learning and associated neural basis, however, remains a topic of debate. Specifically, it is unclear if the initial acquisition of aversive representations of monetary losses depends on similar neural systems as more traditional aversive conditioning that involves primary reinforcers. This study contrasts the efficacy of a biologically defined primary reinforcer (shock) and a socially defined secondary reinforcer (money) during aversive learning and its associated neural circuitry. During a two-part experiment, participants first played a gambling game where wins and losses were based on performance to gain an experimental bank. Participants were then exposed to two separate aversive conditioning sessions. In one session, a primary reinforcer (mild shock) served as an unconditioned stimulus (US) and was paired with one of two colored squares, the conditioned stimuli (CS+ and CS−, respectively). In another session, a secondary reinforcer (loss of money) served as the US and was paired with one of two different CS. Skin conductance responses were greater for CS+ compared to CS− trials irrespective of type of reinforcer. Neuroimaging results revealed that the striatum, a region typically linked with reward-related processing, was found to be involved in the acquisition of aversive conditioned response irrespective of reinforcer type. In contrast, the amygdala was involved during aversive conditioning with primary reinforcers, as suggested by both an exploratory fMRI analysis and a follow-up case study with a patient with bilateral amygdala damage. Taken together, these results suggest that learning about potential monetary losses may depend on reinforcement learning related systems, rather than on typical structures involved in more biologically based fears.

Highlights

  • Monetary rewards are a common reinforcer used in experimental paradigms across a range of disciplines, from behavioral economics to neuropsychological investigations of learning (e.g., Knutson et al, 2003; Delgado et al, 2006; Vohs et al, 2006)

  • Potential monetary losses can modulate decision-making under risk (Kahneman and Tversky, 1979), it is unclear if the initial acquisition of aversive representations of monetary losses depends on overlapping systems as more traditional aversive conditioning that involves primary reinforcers

  • The use of money as an unconditioned stimulus (US) during aversive conditioning led to the expression of a conditioned response, similar to responses elicited by shock, as measured by skin conductance responses (SCRs)

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Summary

Introduction

Monetary rewards are a common reinforcer used in experimental paradigms across a range of disciplines, from behavioral economics to neuropsychological investigations of learning (e.g., Knutson et al, 2003; Delgado et al, 2006; Vohs et al, 2006). The use of monetary reinforcers are of particular interest in experiments that probe the neural correlates of learning and decision-making, since the value of money can be positive or negative depending on the context in which it is presented. Across such studies, the human striatum has been identified as a key region involved in reward-related processing that facilitates reward learning and goal-directed behaviors (Montague and Berns, 2002; Knutson and Cooper, 2005; Delgado, 2007; Rangel et al, 2008). The goal of this study is to provide a direct comparison between a biologically defined primary reinforcer (i.e., shock) and a socially defined secondary reinforcer (i.e., money) and their respective influences in the neural circuits and expression of aversive learning

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