Affective and cognitive mechanisms of risky decision making

Highlights

• Rats chose between small, “safe” rewards and large rewards with risks of shock.

• Choice was more sensitive to shock intensity than reward magnitude.

• Risk averse rats showed less cognitive flexibility than risk taking rats.

• Rats with greater impulsive choice showed worse working memory.

• Risky and impulsive choice are associated with distinct executive functions.

Abstract

The ability to make advantageous decisions under circumstances in which there is a risk of adverse consequences is an important component of adaptive behavior; however, extremes in risk taking (either high or low) can be maladaptive and are characteristic of a number of neuropsychiatric disorders. To better understand the contributions of various affective and cognitive factors to risky decision making, cohorts of male Long-Evans rats were trained in a “Risky Decision making Task” (RDT), in which they made discrete trial choices between a small, “safe” food reward and a large, “risky” food reward accompanied by varying probabilities of footshock. Experiment 1 evaluated the relative contributions of the affective stimuli (i.e., punishment vs. reward) to RDT performance by parametrically varying the magnitudes of the footshock and large reward. Varying the shock magnitude had a significant impact on choice of the large, “risky” reward, such that greater magnitudes were associated with reduced choice of the large reward. In contrast, varying the large, “risky” reward magnitude had minimal influence on reward choice. Experiment 2 compared individual variability in RDT performance with performance in an attentional set shifting task (assessing cognitive flexibility), a delayed response task (assessing working memory), and a delay discounting task (assessing impulsive choice). Rats characterized as risk averse in the RDT made more perseverative errors on the set shifting task than did their risk taking counterparts, whereas RDT performance was not related to working memory abilities or impulsive choice. In addition, rats that showed greater delay discounting (greater impulsive choice) showed corresponding poorer performance in the working memory task. Together, these results suggest that reward-related decision making under risk of punishment is more strongly influenced by the punishment than by the reward, and that risky and impulsive decision making are associated with distinct components of executive function.

Introduction

Decisions among options that vary in both their payoffs and their potential for adverse consequences are a consistent feature of everyday life. When faced with such choices, most individuals can weigh the relative risks and rewards associated with the competing options and decide adaptively; however, such choice behavior (henceforth referred to as “risky decision making”) may be altered in several neuropsychiatric conditions, such that choices are strongly biased toward or away from “risky” options. For example, high levels of risk taking are present in ADHD and addiction, where they may contribute to some of the adverse outcomes associated with these conditions (Bechara et al., 2001, Drechsler et al., 2008, Ernst et al., 2003, Kagan, 1987). In contrast, abnormally low levels of risk taking (risk aversion) are found in anorexia nervosa and social anxiety ((Butler and Mathews, 1987, Kaye et al., 2013, Stanley, 2002) although see (Reynolds et al., 2013)). Hence, a better understanding of the neurobehavioral mechanisms underlying risky decision making may yield benefits across the clinical spectrum.

The current study employed a rat model of risky decision making in which rats make discrete trial choices between a small, “safe” food reward and a large “risky” food reward accompanied by varying probabilities of mild footshock (the “Risky Decision making Task”, or RDT). Previous work has shown that male Long-Evans rats display marked individual variability in their preference for the large, risky reward in this task. Some rats show a strong preference for the large reward even with a high probability of shock (i.e., “risk takers”), whereas other rats show a strong preference for the small reward even when there is a low probability of shock (i.e., “risk averse”) (Simon et al., 2011). These differences in performance are not associated with variability in reward motivation, anxiety, or shock reactivity (Simon et al., 2009, Simon et al., 2011). However, rats with a high preference for risk taking acquire cocaine self-administration more rapidly and have lower striatal dopamine D2 receptor mRNA expression than rats with a low preference for risk taking (Mitchell et al., 2014); Simon et al., 2011). Notably, elevated risk taking in humans is associated with both addiction and reduced striatal D2 receptor availability (Bechara et al., 2001, Goldstein et al., 2009, Rogers et al., 1999, Volkow et al., 2004), supporting the validity of the RDT as a model of human risk taking behavior. The aim of the current study was to assess affective and cognitive mechanisms that may mediate RDT performance, by manipulating the affective value of the RDT task parameters, and by determining associations between risk taking and several measures of executive function. A first cohort of rats was exposed to varying magnitudes of footshock to determine the effects of punishment magnitude on RDT performance. A second cohort was presented with variable numbers of food pellets upon choice of the “risky” option, to determine the effects of reward magnitude on RDT performance. Finally, a third cohort of rats was trained on a set shifting task, a working memory task, the RDT, and a delay discounting task to determine relationships among these different aspects of cognition and decision making.