Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences

Abstract

Background: If presentation of a stimulus (conditional stimulus, CS) reliably predicts delivery of a reward, the CS will come to evoke a conditional response (CR) through Pavlovian learning, and the CS may also acquire incentive motivational properties. Thus, CSs can have both predictive and incentive properties. We ask here whether it is possible to dissociate the predictive versus incentive properties of a CS in rats by considering individual differences in the nature of the CR.

Methods: We used Pavlovian procedures to study the ability of a localizable CS (an illuminated lever) to acquire two properties of an incentive stimulus-the ability to attract and the ability to act as a conditional reinforcer.

Results: For some rats, the CS evoked a "sign-tracking" CR, consisting of approach toward and engagement with the CS itself. For other rats, the CS instead produced a "goal-tracking" CR: approach was directed away from the CS toward the site of food delivery. For sign-trackers (but not goal-trackers) the CS also acted as an effective conditional reinforcer.

Conclusions: The predictive and incentive properties of a CS can be dissociated by considering individual differences in the CR. In a given animal, a cue that is predictive of reward, supporting Pavlovian learning, may or may not be attributed with incentive salience. This procedure may provide a powerful means to test hypotheses regarding the role of neural systems in learning versus incentive motivational functions and to study individual variation in the extent to which reward-associated stimuli act as incentive stimuli.

Figure 1

Individual differences in the development of Pavlovian conditional responses (CRs) due to repeated pairing of a conditional stimulus (CS - an illuminated lever) with delivery of an unconditional stimulus (US - a food pellet). In one group of animals (UN, Unpaired, N = 20) the CS and US were presented pseudo-randomly. After training the “paired” group of animals was subdivided into two groups. The one third of animals that made the highest number of lever contacts were designated sign-trackers (ST, N = 18) and the one third that made the lowest number were designated goal-trackers (GT, N = 18). The panels on the left show three measures of behavior directed towards the lever-CS (sign-tracking behavior). Panel A shows the mean ± SEM probability of approaching the lever during the 8 sec CS period. Panel B shows the mean ± SEM number of lever contacts during the CS period, as indicated by sufficient pressure on the lever to record a “lever press”. Note however that lever contacts were typically caused not by “pressing” the lever with the paws, but by animals vigorously grasping and gnawing on the lever. Panel C shows the mean ± SEM latency to the first lever contact after CS presentation. The panels on the right show three measures of behavior directed towards the place where food will be delivered (goal-tracking behavior). Panel D shows the mean ± SEM probability of approach to the food tray during the 8 sec CS period. Panel E shows the mean ± SEM number of food tray beam breaks during the CS period. Panel F shows the mean ± SEM latency to the first beam break after CS presentation.

Figure 2

Test for conditional reinforcement in the sign-trackers (ST, N = 18), goal-trackers (GT, N = 18) and Unpaired animals (UN, N = 20) described in Fig. 1. On this test a nose poke into one port (active) resulted in presentation of the lever-CS for 2 sec. Nose pokes into the other port (inactive) had no consequence. Panel A shows the mean + SEM number of active and inactive nose pokes for each of the three groups. Panel B shows the number of lever contacts during the entire 40 min test.

Figure 3

Panel A shows the results of Pavlovian training over 22 days (25 trials/day) plotted in 50-trial blocks, in animals designated sign-trackers (ST, N = 10), goal-trackers (GT, N = 10) or the intermediate group (IG, N = 9). Panel A shows only the data for lever contacts, but the rest of the dataset is very similar to that illustrated in Fig. 1, so these data are not shown for the sake of brevity. Panel B shows the relationship between locomotor activity in a novel environment and sign-tracking behavior. Panel C shows the results of the test for conditional reinforcement.

Figure 4

Instrumental learning in sign-trackers (ST), goal-trackers (GT) and unpaired rats (UN). After 8 sessions of Pavlovian training animals were divided into STs (N = 20) and GTs (N = 20) as above. The intermediate third was not tested further in this experiment. However, in a third group of animals (UN, Unpaired, N = 14) the CS and US were presented pseudo-randomly. Panel A shows the data for lever contacts during Pavlovian training. Panel B shows the effects of subsequent instrumental training on an FR-1 schedule of reinforcement for 3 consecutive days. After the third day of testing on an FR-1 schedule the animals were transferred to a VI-5 (variable interval 5 sec) schedule of reinforcement for 3 days (see Panel C).