Pavlovian Conditioned Approach Research Articles

Dissociable deficits of executive function caused by gestational adversity are linked to specific transcriptional changes in the prefrontal cortex.

Poor-quality maternal diet during pregnancy, and subsequent gestational growth disturbances in the offspring, have been implicated in the etiology of multiple neurodevelopmental disorders, including ADHD, schizophrenia, and autism. These disorders are characterized, in part, by abnormalities in responses to reward and errors of executive function. Here, we demonstrate dissociable deficits in reward processing and executive function in male and female mice, solely due to maternal malnutrition via high-fat or low-protein diets. Gestational exposure to a high-fat diet delayed acquisition of a fixed ratio response, and decreased motivation as assessed by progressive ratio. In contrast, offspring of a low-protein diet displayed no deficits in operant learning, but were more prone to assign salience to a cue that predicts reward (sign-tracking) in a Pavlovian-conditioned approach task. In the 5-choice serial reaction time task (5-CSRTT), gestational exposure to a high-fat diet promoted impulsivity, whereas exposure to a low-protein diet led to marked inattention. These dissociable executive function deficits are known to be mediated by the medial prefrontal cortex (PFC), which displays markers of epigenetic dysregulation in neurodevelopmental disorders. Following behavioral characterization, we assayed PFC gene expression using a targeted PCR array and found that both maternal diets increased overall transcription in PFC. Cluster analysis of the relationships between individual transcripts and behavioral outcomes revealed a cluster of primarily epigenetic modulators, whose overexpression was linked to executive function deficits. The overexpression of four genes, DNA methyltransferase 1 (DNMT1), δ-opioid receptor (OPRD1), cannabinoid receptor 1 (CNR1), and catechol-o-methyltransferase (COMT), was strongly associated with overall poor performance. All 5-CSRTT deficits were associated with DNMT1 upregulation, whereas impulsive behavior could be dissociated from inattention by overexpression of OPRD1 or COMT, respectively, as well as a distinct cluster of epigenetic regulators. These data provide molecular support for dissociable domains of executive function.

Individual variation in the propensity to attribute incentive salience to a food cue: Influence of sex

There is considerable individual variation in the propensity of animals to attribute incentive salience to discrete reward cues, but to date most of this research has been conducted in male rats. The purpose of this study was to determine whether sex influences the propensity to attribute incentive salience to a food cue, using rats from two different outbred strains (Sprague-Dawley [SD] and Heterogeneous Stock [HS]). The motivational value of a food cue was assessed in two ways: (i) by the ability of the cue to elicit approach toward it and (ii) by its ability to act as a conditioned reinforcer. We found that female SD rats acquired Pavlovian conditioned approach behavior slightly faster than males, but no sex difference was detected in HS rats, and neither strain showed a sex difference in asymptotic performance of approach behavior. Moreover, female approach behavior did not differ across estrous cycle. Compared to males, females made more active responses during the test for conditioned reinforcement, although they made more inactive responses as well. We conclude that although there are small sex differences in performance on these tasks, these are probably not due to a notable sex difference in the propensity to attribute incentive salience to a food cue.

Effects of ethanol exposure during adolescence or in adulthood on Pavlovian conditioned approach in Sprague-Dawley rats

Human studies have shown that adolescents who repeatedly use alcohol are more likely to be dependent on alcohol and are more likely to suffer from psychological problems later in life. There has been limited research examining how ethanol exposure in adolescence might contribute to later abuse or addiction in adulthood. The present experiment examined effects of intermittent ethanol exposure during adolescence on sign-tracking behavior in adulthood, indexed by a Pavlovian conditioned approach (PCA) task wherein an 8s lever presentation served as a cue predicting subsequent delivery of a flavored food pellet. Although no response was required for food delivery, after multiple pairings, 1 of 2 different responses often emerged during the lever presentation: goal tracking (head entries into the food trough) or sign tracking (engagement with the lever when presented). Sign tracking is thought to reflect the attribution of incentive salience to reward-paired cues and has been previously correlated with addiction-like behaviors. Following the last PCA session, blood samples were collected for analysis of post-session corticosterone levels. Sixty-two rats (n = 10–12/group) were pseudo-randomly assigned to 1 of 2 intragastric (i.g.) exposure groups (water or 4 g/kg ethanol) or a non-manipulated (NM) control group. Animals were intubated with ethanol or water every other session from postnatal session (PND) 28–48 or PND 70–90. Rats were then tested in adulthood (PND 71–79 or PND 113–122) on the PCA task. Animals exposed chronically to ethanol during adolescence exhibited significantly higher levels of sign-tracking behavior in adulthood than NM and water-treated animals, and showed higher corticosterone than NM control animals. These effects were not seen after comparable ethanol exposure in adulthood. These results suggest that adolescent alcohol exposure has long-term consequences on the expression of potential addiction-relevant behaviors in adulthood.

Sign-tracking to an appetitive cue predicts incubation of conditioned fear in rats

Although post-traumatic stress disorder (PTSD) and addiction are very different disorders, both are characterized by hyperreactivity to trauma- or drug-related cues, respectively. We investigated whether an appetitive conditioning task, Pavlovian conditioned approach, which predicts vulnerability to reinstatement of cocaine-seeking, also predicts fear incubation, which may be a marker for vulnerability to PTSD. We classified rats based on whether they learned to approach and interact with a food predictive cue (sign-trackers), or, whether upon cue presentation they went to the location of impending food delivery (goal-trackers). Rats were then exposed to extensive Pavlovian tone-shock pairings, which causes the fear response to increase or “incubate” over time. We found that the fear incubation effect was only present in sign-trackers. The behavior of goal-trackers was more consistent with a normal fear response–it was most robust immediately after training and decayed slowly over time. Sign-trackers also had lower levels of brain-derived neurotrophic factor (BDNF) protein in the prefrontal cortex than goal-trackers. These results indicate that, while many factors likely contribute to the disproportionate co-occurrence of PTSD and substance abuse, one such factor may be a core psychological trait that biases some individuals to attribute excessive motivational significance to predictive cues, regardless of the emotional valence of those cues. High levels of BDNF in the prefrontal cortex may be protective against developing excessive emotional and motivational responses to salient cues.

Dorsal hippocampus inactivation impairs spontaneous recovery of Pavlovian magazine approach responding in rats

Destruction or inactivation of the dorsal hippocampus (DH) has been shown to eliminate the renewal of extinguished fear [1–4]. However, it has recently been reported that the contextual control of responding to extinguished appetitive stimuli is not disrupted when the DH is destroyed or inactivated prior to tests for renewal of Pavlovian conditioned magazine approach [5]. In the present study we extend the analysis of DH control of appetitive extinction learning to the spontaneous recovery of Pavlovian conditioned magazine approach responding. Subjects were trained to associate two separate stimuli with the delivery of food and had muscimol or vehicle infused into the DH prior to a single test-session for spontaneous recovery occurring immediately following extinction of one of these stimuli, but one week following extinction of the other. While vehicle treated subjects showed more recovery to the distally extinguished stimulus than the proximal one, muscimol treated subjects failed to show spontaneous recovery to either stimulus. This result suggests that, while the DH is not involved in the control of extinction by physical contexts [5], it may be involved when time is the gating factor controlling recovery of extinguished responding.

Modelling individual differences in the form of Pavlovian conditioned approach responses: a dual learning systems approach with factored representations.

Reinforcement Learning has greatly influenced models of conditioning, providing powerful explanations of acquired behaviour and underlying physiological observations. However, in recent autoshaping experiments in rats, variation in the form of Pavlovian conditioned responses (CRs) and associated dopamine activity, have questioned the classical hypothesis that phasic dopamine activity corresponds to a reward prediction error-like signal arising from a classical Model-Free system, necessary for Pavlovian conditioning. Over the course of Pavlovian conditioning using food as the unconditioned stimulus (US), some rats (sign-trackers) come to approach and engage the conditioned stimulus (CS) itself – a lever – more and more avidly, whereas other rats (goal-trackers) learn to approach the location of food delivery upon CS presentation. Importantly, although both sign-trackers and goal-trackers learn the CS-US association equally well, only in sign-trackers does phasic dopamine activity show classical reward prediction error-like bursts. Furthermore, neither the acquisition nor the expression of a goal-tracking CR is dopamine-dependent. Here we present a computational model that can account for such individual variations. We show that a combination of a Model-Based system and a revised Model-Free system can account for the development of distinct CRs in rats. Moreover, we show that revising a classical Model-Free system to individually process stimuli by using factored representations can explain why classical dopaminergic patterns may be observed for some rats and not for others depending on the CR they develop. In addition, the model can account for other behavioural and pharmacological results obtained using the same, or similar, autoshaping procedures. Finally, the model makes it possible to draw a set of experimental predictions that may be verified in a modified experimental protocol. We suggest that further investigation of factored representations in computational neuroscience studies may be useful.

Erratum to: Pavlovian conditioned approach, extinction, and spontaneous recovery to an audiovisual cue paired with an intravenous heroin infusion

Erratum to: Pavlovian conditioned approach, extinction, and spontaneous recovery to an audiovisual cue paired with an intravenous heroin infusion

Variation in the form of Pavlovian conditioned approach behavior among outbred male Sprague-Dawley rats from different vendors and colonies: sign-tracking vs. goal-tracking.

Even when trained under exactly the same conditions outbred male Sprague-Dawley (SD) rats vary in the form of the Pavlovian conditioned approach response (CR) they acquire. The form of the CR (i.e. sign-tracking vs. goal-tracking) predicts to what degree individuals attribute incentive salience to cues associated with food or drugs. However, we have noticed variation in the incidence of these two phenotypes in rats obtained from different vendors. In this study, we quantified sign- and goal-tracking behavior in a reasonably large sample of SD rats obtained from two vendors (Harlan or Charles River), as well as from individual colonies operated by both vendors. Our sample of rats acquired from Harlan had, on average, more sign-trackers than goal-trackers, and vice versa for our sample of rats acquired from Charles River. Furthermore, there were significant differences among colonies of the same vendor. Although it is impossible to rule out environmental variables, SD rats at different vendors and barriers may have reduced phenotypic heterogeneity as a result of genetic variables, such as random genetic drift or population bottlenecks. Consistent with this hypothesis, we identified marked population structure among colonies from Harlan. Therefore, despite sharing the same name, investigators should be aware that important genetic and phenotypic differences exist among SD rats from different vendors or even from different colonies of the same vendor. If used judiciously this can be an asset to experimental design, but it can also be a pitfall for those unaware of the issue.

Environmental manipulations alter age differences in attribution of incentive salience to reward-paired cues

Cues repeatedly paired with rewards often themselves become imbued with enhanced motivational value, or incentive salience. During Pavlovian conditioned approach procedures, a cue repeatedly preceding reward delivery often elicits conditioned responses at either the reward delivery location (“goal-tracking”) or the cue itself (“sign-tracking”). Sign-tracking behavior is thought to reflect the individual differences in attribution of incentive salience to reward-paired cues that may contribute to addiction vulnerability. Adolescent rats typically demonstrate less sign-tracking behavior than adult rats, a surprising finding given that adolescence is hypothesized to be a time of heightened addiction vulnerability. Given evidence that adult sign-tracking behavior can be influenced by environmental conditions, the present study compared the effects of isolate housing and food deprivation on expression of sign-tacking and goal-tracking behavior in adolescent and adult male rats across eight days of a Pavlovian conditioned approach procedure. Pair-housed adults exhibited more sign-tracking behavior than pair-housed adolescents; however, this age difference was not apparent in isolate-housed subjects. Adolescents often appeared more sensitive than adults to both food restriction- and isolate housing-induced changes in behavior, with food restriction promoting an increase in sign-tracking among isolate-housed adolescents and an increase in goal-tracking among pair-housed adolescents. For adults, food restriction resulted in a modest increase in overall expression of both sign- and goal-tracking behavior. To the extent that sign-tracking behavior reflects attribution of incentive salience to reward-paired cues, results from the present study provide evidence that reactivity to rewards during adolescence is strongly related to the nature of the surrounding environment.

Pavlovian conditioned approach, extinction, and spontaneous recovery to an audiovisual cue paired with an intravenous heroin infusion

Novel stimuli paired with exposure to addictive drugs can elicit approach through Pavlovian learning. While such approach behavior, or sign tracking, has been documented for cocaine and alcohol, it has not been shown to occur with opiate drugs like heroin. Most Pavlovian conditioned approach paradigms use an operandum as the sign, so that sign tracking can be easily automated. We were interested in assessing whether approach behavior occurs to an audiovisual cue paired with an intravenous heroin infusion. If so, would this behavior exhibit characteristics of other Pavlovian conditioned behaviors, such as extinction and spontaneous recovery? Rats were repeatedly exposed to an audiovisual cue, similar to that used in standard self-administration models, along with an intravenous heroin infusion. Sign tracking was measured in an automated fashion by analyzing motion pixels within the cue zone during each cue presentation. We were able to observe significant sign tracking after only five pairings of the conditioned stimulus (CS) with the unconditioned stimulus (US). This behavior rapidly extinguished over 2days, but exhibited pronounced spontaneous recovery 3weeks later. We conclude that sign tracking measured by these methods exhibits all the characteristics of a classically conditioned behavior. This model can be used to examine the Pavlovian component of drug memories, alone, or in combination with self-administration methods.

Age Differences in Ethanol Discrimination: Acquisition and Ethanol Dose Generalization Curves Following Multiple Training Conditions in Adolescent and Adult Rats

Adolescents and adults vary in sensitivity to many effects of ethanol (EtOH), although it is unknown whether they also differ in their perception of EtOH's subjective cues. This study characterized EtOH discrimination in adolescent and adult male rats using a rapidly acquired Pavlovian conditioned approach procedure. EtOH at 1 of the 3 training doses (0.75, 1.0, or 1.25 g/kg) served as either a positive (POS) or negative (NOS) occasion setter. Each 20-minute training session consisted of eight 15-second presentations of 2 cue lights located on either side of a dipper delivering chocolate Boost(®) . For POS-trained rats, the cue lights reliably predicted 5-second presentations of chocolate Boost during EtOH but not saline sessions, with the opposite contingencies used for NOS-trained rats. Anticipatory approach behavior (head entries into the reward delivery area) in the presence and absence of the cue lights was used to calculate discrimination scores on EtOH and saline sessions. Following acquisition, various doses of EtOH (0 to 1.5 g/kg) were administered to establish generalization curves. Although animals of both ages responded differentially on EtOH and saline sessions by the end of acquisition, adults met criterion more quickly and had higher discrimination scores during reinforced sessions than adolescents. Whereas adolescents failed to demonstrate any dose-dependent responding during testing when trained with the 0.75 or 1.25 g/kg EtOH doses, adults demonstrated broader EtOH generalization during testing sessions following training with all 3 EtOH doses. Among adolescents trained with 1.0 g/kg EtOH, less generalization occurred relative to adults. Adolescents were less sensitive to EtOH's interoceptive effects, indicating that EtOH is likely a more salient cue for adults than for adolescents. These findings contribute to evidence that suggests adolescent-typical insensitivity to internal cues that typically limit EtOH consumption may contribute to the elevated intake commonly reported during this developmental period.

Genetic Reconstruction of Dopamine D1 Receptor Signaling in the Nucleus Accumbens Facilitates Natural and Drug Reward Responses

The dopamine D1 receptor (D1R) facilitates reward acquisition and its alteration leads to profound learning deficits. However, its minimal functional circuit requirement is unknown. Using conditional reconstruction of functional D1R signaling in D1R knock-out mice, we define distinct requirements of D1R in subregions of the nucleus accumbens (NAc) for specific dimensions of reward. We demonstrate that D1R expression in the core region of the NAc (NAc(Core)), but not the shell (NAc(Shell)), enhances selectively a unique form of pavlovian conditioned approach and mediates D1R-dependent cocaine sensitization. However, D1R expression in either the NAc(Core) or the NAc(Shell) improves instrumental responding for reward. In contrast, neither NAc(Core) nor NAc(Shell) D1R is sufficient to promote motivation to work for reward in a progressive ratio task or for motor learning. These results highlight dissociated circuit requirements of D1R for dopamine-dependent behaviors.

Appetitive Pavlovian goal-tracking memories reconsolidate only under specific conditions

Despite extensive evidence that appetitive memories undergo reconsolidation, two notable failures to observe reconsolidation have been reported: instrumental responding and goal-tracking. However, these studies do not provide conclusive evidence for a lack of memory reconsolidation due to the numerous boundary conditions that dictate whether a memory will undergo reconsolidation. In this study we sought to reexamine reconsolidation in an appetitive, Pavlovian conditioned approach procedure and the behavioral boundary conditions within which memories are destabilized and reconsolidated. This study demonstrated that a Pavlovian goal-tracking memory, previously thought to be resistant to destabilization, will undergo memory reconsolidation under discrete conditions that favor reconsolidation as opposed to extinction, and that this is dependent on the amount of training rats received. With restricted training, systemic administration of MK-801 impaired memory extinction. In contrast, with more extended training, MK-801 administration impaired memory reconsolidation. We also demonstrate that behavioral boundary conditions that exist for appetitive memory reconsolidation are much more complex than simple parametric calculations. Moreover, extinction per se is not a boundary on reconsolidation, in that MK-801 also has no behavioral effect under some conditions.

Over-expectation generated in a complex appetitive goal-tracking task is capable of inducing memory reconsolidation

Discrepancies in an expected outcome have been demonstrated to result in modification of behaviour in both appetitive and aversive conditioning settings. In this study, we sought to establish whether overexpectation generated from compound conditioning with two previously rewarded stimuli was able to induce memory destabilisation and subsequent reconsolidation in a Pavlovian conditioned approach setting. It was shown that 4 days, but not 1 day, of overexpectation training was required to induce memory reconsolidation, and this was disrupted by application of the NMDA subtype of glutamate receptor antagonist MK-801 prior to overexpectation training, but not by MK-801 application 6 h post-training. These data provide evidence that the memories underlying Pavlovian conditioned approach do undergo reconsolidation and that such reconsolidation can be triggered by overexpectation. Therefore, the updating of appetitive conditioned stimulus and unconditioned stimulus associations underpinning conditioned responding in manners other than extinction training is likely achieved through memory reconsolidation.

A classically conditioned cocaine cue acquires greater control over motivated behavior in rats prone to attribute incentive salience to a food cue

Cues associated with rewards bias attention towards them and can motivate drug-seeking and drug-taking behavior. There is, however, considerable individual variation in the extent to which cues associated with rewards acquire motivational properties. For example, only in some rats does a localizable food cue become attractive, eliciting approach towards it, and "wanted", in the sense that it serves as an effective conditioned reinforcer. We asked whether the propensity of animals to attribute incentive salience to a food cue predicts the extent to which a classically conditioned cocaine cue acquires incentive motivational properties. First, a Pavlovian conditioned approach procedure was used to identify rats prone to attribute incentive salience to a food cue. We then measured the extent to which a classically conditioned cocaine cue acquired two properties of an incentive stimulus: (1) the ability to elicit approach towards it, and (2) the ability to reinstate drug-seeking behavior, using an extinction-reinstatement procedure (i.e., to act as a conditioned reinforcer). We found that a classically conditioned cocaine cue became more attractive, in that it elicited greater approach toward it, and more desired, in that it supported more drug-seeking behavior under extinction conditions, in individuals prone to attribute incentive salience to a food cue. We conclude that rats vary in their propensity to attribute incentive salience to both food and cocaine cues, and it is possible to predict, prior to any drug experience, in which rats a cocaine cue will acquire the strongest motivational control over behavior.

The effect of nicotine on sign-tracking and goal-tracking in a Pavlovian conditioned approach paradigm in rats

Nicotine (NIC) potently increases operant responding for non-NIC reinforcers, and this effect may depend on drug-mediated increases in incentive motivation. According to this hypothesis, NIC should also potently increase approach to Pavlovian-conditioned stimuli associated with rewards. The present studies explored the effects of NIC on Pavlovian-conditioned approach responses. To do so, liquid dippers were used to deliver an unconditioned stimulus (US; 0.1ml sucrose) after presentation of a conditioned stimulus (CS; 30s illumination of a stimulus light)-both the CS and US were presented in receptacles equipped to monitor head entries. In experiment 1, the CS and US were presented in the same receptacle, but NIC pretreatment (0.4mg/kg base) did not increase conditioned approach responses. Delivery of the sucrose US was then shifted to receptacle in a different location. All rats learned to approach the new US location (goal-tracking) at similar rates. Approach to the CS receptacle (sign-tracking) declined for saline-pretreated rats, but NIC pretreatment increased sign-tracking. In experiment 2, NIC pretreatment increased sign-tracking when the CS and US were spatially separated during acquisition. In experiment 3, NIC pretreatments were replaced with saline, but the effect of NIC persisted for an additional 24 test sessions. The findings suggest that NIC increases incentive motivation and that this effect is long-lasting, persisting beyond the pharmacological effects of NIC.

The role of dopamine in the accumbens core in the expression of Pavlovian‐conditioned responses

The role of dopamine in reward is a topic of debate. For example, some have argued that phasic dopamine signaling provides a prediction-error signal necessary for stimulus-reward learning, whereas others have hypothesized that dopamine is not necessary for learning per se, but for attributing incentive motivational value ('incentive salience') to reward cues. These psychological processes are difficult to tease apart, because they tend to change together. To disentangle them we took advantage of natural individual variation in the extent to which reward cues are attributed with incentive salience, and asked whether dopamine (specifically in the core of the nucleus accumbens) is necessary for the expression of two forms of pavlovian-conditioned approach behavior--one in which the cue acquires powerful motivational properties (sign-tracking) and another closely related one in which it does not (goal-tracking). After acquisition of these conditioned responses (CRs), intra-accumbens injection of the dopamine receptor antagonist flupenthixol markedly impaired the expression of a sign-tracking CR, but not a goal-tracking CR. Furthermore, dopamine antagonism did not produce a gradual extinction-like decline in behavior, but maximally impaired expression of a sign-tracking CR on the very first trial, indicating the effect was not due to new learning (i.e. it occurred in the absence of new prediction-error computations). The data support the view that dopamine in the accumbens core is not necessary for learning stimulus-reward associations, but for attributing incentive salience to reward cues, transforming predictive conditional stimuli into incentive stimuli with powerful motivational properties.

Motivational Mechanisms and Outcome Expectancies Underlying the Approach Bias toward Addictive Substances

Human behavior can be paradoxical, in that actions can be initiated that are seemingly incongruent with an individual’s explicit desires. This is most commonly observed in drug addiction, where maladaptive behavior (i.e., drug seeking) appears to be compulsive, continuing at great personal cost. Approach biases toward addictive substances have been correlated with actual drug-use in a number of studies, suggesting that this measure can, in some cases, index everyday maladaptive tendencies. At present it is unclear whether this bias to drug cues is a Pavlovian conditioned approach response, a habitual response, the result of a Pavlovian-instrumental transfer process, or a goal-directed action in the sense that expectancy of the rewarding effects of drugs controls approach. We consider this question by combining the theoretical framework of associative learning with the available evidence from approach bias research. Although research investigating the relative contributions of these mechanisms to the approach bias is to date relatively limited, we review existing studies and also outline avenues for future research.

Pairings of lever and food induce Pavlovian conditioned approach of sign-tracking and goal-tracking in C57BL/6 mice

In rats, Pavlovian sign-tracking has been extensively evaluated as a model of compulsiveness in drug addiction and other addictive behaviors, but it remains unexplored in mice, a species with a wealth of genetically modified models, which makes it possible to examine gene-behavior relationships. In C57BL/6 mice, the most commonly used mouse strain for genetic studies, repeated pairings of lever conditioned stimulus (CS) with food unconditioned stimulus (US) induced Pavlovian conditioning of sign-tracking conditioned response (ST CR) performance of lever CS-directed approach, and Pavlovian conditioning of goal-tracking conditioned response (GT CR) performance of approach responses directed at the location of the food trough where the food US was delivered. The CS–US Paired group performed more ST CRs and more GT CRs during sessions 15–16 than did pseudoconditioning controls which received the lever CS and food US randomly with respect to one another. During sessions 15–16, all mice in the Paired group performed more GT CRs than ST CRs, and regression analysis revealed a positive relationship between an individual subject's tendency to perform ST CRs and GT CRs. The mice that performed more ST CRs during sessions 15–16 yielded higher plasma corticosterone levels. These data reveal stable and reliable acquisition and maintenance of ST CR performance and GT CR performance in mice; however, unlike in rats, ST CRs and GT CRs did not vary inversely within subjects. Corticosterone release, a pathophysiological marker of vulnerability to drug abuse, was positively related to ST CR performance.

Environmental enrichment reduces attribution of incentive salience to a food-associated stimulus

Animals reared in an enriched environment are less vulnerable to abuse-like behavior and exhibit less persistent drug seeking, perhaps due to a decrease in the incentive value of stimuli associated with reward. The present study investigated the effects of environmental enrichment on Pavlovian conditioned approach (PCA) performance, a measure of incentive salience attribution. Rats were first reared from postnatal day 21 to postnatal day 51 in either an enriched environment with large cages, social cohorts and novel objects, or in an isolated environment with small, hanging cages, no social cohorts and no novel objects. Rats were then trained on a PCA task for 5 consecutive days, where a retractable lever was predictive of a food reward. Isolated rats predominantly exhibited sign-tracking responses directed toward the reward-predicted lever (indicative of incentive salience attribution), while enriched rats predominantly exhibited goal-tracking responses directed toward the location of food delivery. Both groups learned their respective response type at equal rates. The results indicate that environmental enrichment reduces the readiness to attribute incentive value to reward-associated cues, which may explain the enrichment-induced protection against addiction-like behaviors.