Rats prone to attribute incentive salience to reward cues are also prone to impulsive action

Abstract

Animals vary considerably in the degree to which they attribute incentive salience to cues predictive of reward. When a discrete cue (conditional stimulus) is repeatedly paired with delivery of a food reward (unconditional stimulus) only some rats (“sign-trackers”; STs) come to find the cue itself an attractive and desirable incentive stimulus. For other rats (“goal-trackers”; GTs) the cue is an effective conditional stimulus – it evokes a conditional response – but it is less attractive and less desirable. Given that STs have particular difficulty resisting reward cues, and are thought to have poor inhibitory control over their behavior, we hypothesized that they may also be more impulsive. There are, however, multiple forms of impulsivity; therefore, we compared STs and GTs on two tests of so-called impulsive action – a 2-choice serial reaction time task and a differential reinforcement of low rates of responding task, and one test of impulsive choice – a delay discounting choice procedure. We found that relative to GTs, STs were more impulsive on the two tests of impulsive action, but not on the test of impulsive choice. We speculate that when these two traits combine, that is, when an individual is not only prone to attribute incentive salience to reward cues but also prone to impulsive action, they may be especially susceptible to impulse control disorders, including addiction.

Introduction

Cues associated with rewards (conditional stimuli, CSs) not only evoke conditional responses (CRs), but they can also become attractive and desirable in their own right, acting as incentive stimuli [4], [5], [9], [31]. There is, however, considerable individual variation in the extent to which CSs are attributed with incentive salience, and thus come to motivate behavior. For example, when a spatially discrete cue (a lever) is paired with delivery of a food reward (the unconditional stimulus, US) only in some rats does the lever-CS itself become attractive, eliciting approach towards it [20], [41], and desirable, in that rats will work to get it [37]. These rats are called sign-trackers (STs) because they tend to approach the cue or “sign” that predicts reward [25]. In the same situation other rats, called “goal-trackers” (GTs), do not approach the lever-CS, but CS presentation instigates approach towards the location of food delivery [6], and in GTs, a lever-CS is not a potent conditional reinforcer [37]. Furthermore, both food and cocaine cues are more effective in reinstating seeking for their respective rewards, following extinction, in STs than GTs [39], [53]. Therefore, although reward cues can act as an effective CS for both STs and GTs, they seem to acquire potent incentive properties only in STs [37]. Given their difficulty resisting drug cues, we, and others, have argued that STs may be especially vulnerable to impulse control disorders, including addiction [21], [39], [43].

Another trait thought to confer vulnerability to addiction is impulsivity [13], [14], [15], [28], [35], [48], [52], a hypothesis supported by recent preclinical studies. For example, high-impulsive rats are more likely to compulsively self-administer drugs than low-impulsive rats [3] and are more likely to show reinstatement of drug-seeking following punishment-induced extinction [18]. Interestingly, it has been argued that STs may also have poor inhibitory control over their behavior, and are especially impulsive [22], [43], but there are very few studies exploring this topic. Therefore, the purpose of the experiments reported here was to better characterize the relationship between the propensity to attribute incentive salience to a reward cue and the propensity to be impulsive.

Impulsivity is characterized by premature actions, reduced tolerance of delay of gratification and rapid decision-making, and therefore, is not a unitary construct [19]. It has been suggested that forms of impulsivity can be grouped into at least two broad dissociable classes: impulsive action and impulsive choice [15], [16], [19], [33], [34], [50]. Impulsive action refers to phenomena where an individual fails to inhibit premature or poorly timed responses, whereas impulsive choice refers to situations where an organism is faced with action choices, each leading to distinct outcomes [1], [10], [14], [19], [27], [33]. Therefore, we tested STs and GTs on two tests thought to be sensitive to impulsive action, a differential reinforcement of low rates of responding (DRL) task and a 2-choice serial reaction time task (2-CSRTT; a simplified version of 5-CSRTT), as well as a test of so-called impulsive choice, a delay discounting (DD) choice task. We report that, relative to GTs, STs are prone to make impulsive actions, but not impulsive choices.