Research reportRats prone to attribute incentive salience to reward cues are also prone to impulsive action
Highlights
► We examine the relationship between two ‘traits’ linked to addiction. ► We find that rats prone to attribute incentive salience to reward cues are also prone to impulsive action. ► We propose that individuals scoring high on both traits will be most susceptible to 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.
Section snippets
Subjects
Male Sprague–Dawley rats (Harlan, IN) were used, and different rats were used in three independent experiments. Upon arrival, rats (∼60 days old; ∼280 g) were housed individually in Plexiglas cages (W 26 × L 38 × H 21 cm), lined with bedding (Bed O’Cobs®), in a temperature- and humidity-controlled room (22 ± 1 °C and 40–50%, respectively) with lights off from 2000 to 0800 h. Rats had ad lib access to Purina rat chow (unless otherwise specified, see below) and water. All testing was done between 0900 and
Pavlovian conditioned approach
Fig. 1 shows the change in PCA index scores over the 5 days of Pavlovian training in rats classed as STs or GTs based on their performance on days 4 and 5 of training. As would be expected, there was a significant main effect of group [F(1, 85) = 636.1, p < 0.0001], and session [F(4, 332) = 17.79, p < 0.0001], and a significant group × session interaction [F(4, 332) = 91.13, p < 0.0001]. Fig. 2 shows the performance of STs and GTs across days of training on three measures of Pavlovian approach. With training
Discussion
We asked whether rats that are prone to attribute incentive salience to reward cues (STs) are also impulsive, as indicated by tests of so-called impulsive action and impulsive choice [14], [19], [33]. We found that, relative to GTs, STs had difficulty withholding a response when required to do so to receive an impending reward, as indicated by more premature responses on both the DRL task and 2-CSRTT. In contrast, at the longest delay interval, STs were more likely than GTs to choose a larger
Disclosure
The authors declare no conflict of interest.
Acknowledgements
This research was supported by a grant from the National Institute on Drug Abuse (R37 DA04294) to TER. We thank Alex Belakovskiy and Tony McClafferty for technical assistance.
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