An omission procedure reorganizes the microstructure of sign-tracking while preserving incentive salience

Abstract

Appetitive sign-tracking, in which reward-paired cues elicit approach that can result in cue interaction, demonstrates how cues acquire motivational value. For example, rats will approach and subsequently interact with a lever insertion cue that signals food delivery upon its retraction. However, lever deflections are rapidly reduced once rats are trained on an omission schedule in which lever interactions cancel food delivery. Here we evaluated the change in sign-tracking response topography in rats exposed to such an omission procedure. Lever deflections dropped precipitously when they canceled reward. However, rats that were on an omission schedule continued to approach, sniff, and contact the lever without pressing it, and did so at comparable rates to rats that were not under an omission schedule. Thus, sign-tracking was maintained, albeit in a different manner, following omission. Such findings show that the motivational attraction to reward cues can be expressed with remarkable persistence and flexibility.[Supplemental material is available for this article.]Appetitive sign-tracking is a phenomenon in which a rewardpaired cue elicits approach that can result in cue interaction (Brown and Jenkins 1968;Jenkins and Moore 1973;Hearst and Jenkins 1974;Boakes 1977). For example, rats will acquire a conditioned response (CR) in which they will approach, contact, and bite a lever conditioned stimulus (CS) that signals the delivery of a food unconditioned stimulus (US). Sign-tracking is a key model for studying behavioral and neural mechanisms of normal and excessive motivational attraction to reward-paired stimuli (Lajoie and Bindra 1976;Berridge 2004;Tomie et al. 2008;Flagel et al. 2010;Robinson and Berridge 2013;Huys et al. 2014;Robinson et al. 2014).Negative automaintenance, in which a lever press cancels reward, has been used to show that sign-tracking can be markedly sensitive to instrumental contingency changes (Williams and Williams 1969;Stiers and Silberberg 1974;Locurto et al. 1976), suggesting a sensitivity to response-reward associations (Skinner 1992). For example, Locurto et al. (1976) have found that lever contacts after sign-tracking are markedly reduced in rats moved to an omission schedule, with similar rates of lever contacts compared with rats exposed to extinction or random cue/reward delivery. However, typically, sign-tracking does not decline to zero (Atnip 1977;Eldridge and Pear 1987;Schwartz and Williams 1972a;Stiers and Silberberg 1974;Woodard et al. 1974), suggesting some motivational persistence as well. Thus, sign-tracking CRs may be partly sensitive to contingency and partly under control of motivational forces that promote its persistence.Generally, it remains unclear to what quantitative extent the motivational attraction to the CS actually declines along with the declining CR when it cancels reward. Is the incentive value of the CS retained but masked by reduced lever pressing measures, or is it reduced as well?To clarify this issue, we studied the response topography of sign-trac...

Long‐lasting contribution of dopamine in the nucleus accumbens core, but not dorsal lateral striatum, to sign‐tracking

“…Interestingly, sign-tracking, a Pavlovian conditioned response, shares many behavioral features of instrumental behaviors that have been described as habitual. For example, sign-tracking is resistant to outcome devaluation (Morrison et al, 2015;Nasser et al, 2015;Patitucci et al, 2016) and extinction (Ahrens et al, 2016), persists following response-dependent omission of reward (Chang & Smith, 2016), and behavioral inflexibility predicts the degree to which a rat sign-tracks (Nasser et al, 2015). However, sign-tracking differs in that it can be immediately produced following a shift in motivational state which suggests different systems distinguish sign-tracking from instrumental habits at a neural and behavioral level (Robinson & Berridge, 2013;Dayan & Berridge, 2014).…”

Optogenetic activation of amygdala projections to nucleus accumbens can arrest conditioned and unconditioned alcohol consummatory behavior

“…Second, although photoactivation interrupted alcohol drinking, animals continued to interact with the sipper tube during the alcohol drinking test. These within-test dissociations are intriguing and raise important questions about control over the sequence of reward-seeking actions, specifically between approach and “terminal”, consummatory, responses, which are proposed to engage different learning systems (Chang and Smith, 2016; Naeem and White, 2016; Selleck and Baldo, 2017). The findings suggest the interesting possibility that consummatory responses/terminal responses, may be more sensitive to the influence of BLA-AcbSh innervation than more distal actions within the behavioral chain, a possibility awaiting future testing.…”

Neurobiological basis of individual variation in stimulus-reward learning

“…Sign-trackers are also more resistant to extinction of their CR than GTs [18] and will continue to approach the CS even if contact with it results in omission of the reward [19], indicating that approach behavior is not contingent upon subsequent food delivery or maintained via response reinforcement processes [20]. It has also been shown that sign-tracking behavior becomes more pronounced when the relationship between the CS and the reward is uncertain, such that the probability of the reward following CS presentation changes [21].…”