Sign-tracking behavior is sensitive to outcome devaluation in a devaluation context-dependent manner: implications for analyzing habitual behavior

Abstract

Motivationally attractive cues can draw in behavior in a phenomenon termed incentive salience. Incentive cue attraction is an important model for animal models of drug seeking and relapse. One question of interest is the extent to which the pursuit of motivationally attractive cues is related to the value of the paired outcome or can become unrelated and habitual. We studied this question using a sign-tracking (ST) paradigm in rats, in which a lever stimulus preceding food reward comes to elicit conditioned lever-interaction behavior. We asked whether reinforcer devaluation by means of conditioned taste aversion, a classic test of habitual behavior, can modify ST to incentive cues, and whether this depends upon the manner in which reinforcer devaluation takes place. In contrast to several recent reports, we conclude that ST is indeed sensitive to reinforcer devaluation. However, this effect depends critically upon the congruence between the context in which taste aversion is learned and the context in which it is tested. When the taste aversion successfully transfers to the testing context, outcome value strongly influences ST behavior, both when the outcome is withheld (in extinction) and when animals can learn from outcome feedback (reacquisition). When taste aversion does not transfer to the testing context, ST remains high. In total, the extent to which ST persists after outcome devaluation is closely related to the extent to which that outcome is truly devalued in the task context. We believe this effect of context on devaluation can reconcile contradictory findings about the flexibility/inflexibility of ST. We discuss this literature and relate our findings to the study of habits generally.

Figure 1.

ST behavior was sensitive to outcome devaluation. (A) Timeline of experimental procedures: magazine training (Mag), predevaluation extinction session (E1), predevaluation reacquisition session (R1), postdevaluation extinction session (E2), and postdevaluation extinction session (R2). (B) Sign-tracking behavior did not differ between groups on a discriminative sign-tracking protocol over the course of 12 training sessions. Groups readily discriminated between the CS+ and CS− and adjusted responding (presses per minute, ppm) accordingly. (C) Outcome devaluation conducted over the course of five sessions. Sessions 1 and 2, to the left of the dashed line, were conducted in external holding chambers distinct from operant chambers. Sessions 3 and 4 were conducted in operant chambers. Session 5, to the right of the solid line, was conducted in operant chambers but no lithium chloride was administered following pellet presentation as minimal pellets were consumed. (D) Sign-tracking rates (ppm) during 5-min extinction tests pre- and postdevaluation show that Group LiCl-Pellet significantly decreased sign-tracking to the lever following devaluation. (E) Sign-tracking rates (ppm) during fully rewarded sessions show the same drop following outcome devaluation in Group LiCl-Pellet. (F) Pellet consumption during the pre- and postdevaluation reacquisition sessions. Predevaluation, all animals consumed all pellets, as expected. Postdevaluation, animals in Group Saline-Pellet continued to consume all pellets while animals in Group LiCl-Pellet significantly decreased pellet consumption, indicating that outcome devaluation was successful.

Figure 2.

ST sensitivity to outcome devaluation was not a product of generalized negative affect following outcome devaluation. (A) Timeline of experimental procedures: magazine training (Mag), predevaluation extinction session (E1), predevaluation reacquisition session (R1), postdevaluation extinction session (E2), and postdevaluation extinction session (R2). (B) Sign-tracking behavior did not differ between groups on a discriminative sign-tracking protocol over the course of 12 training sessions. Groups readily discriminated between the CS+ and CS− and adjusted responding (presses per minute, ppm) accordingly. (C) Outcome devaluation conducted over the course of five sessions. Sessions 1 and 2, to the left of the dashed line, were conducted in external holding chambers distinct from operant chambers. Sessions 3 and 4 were conducted in operant chambers. Session 5, to the right of the solid line, was conducted in operant chambers but no lithium chloride was administered following pellet presentation as no pellets were consumed. Note that there is no line denoting the control group consumption as no pellets were presented to Group LiCl only during this phase of the experiment. (D) Sign-tracking rates (ppm) during 5-min extinction tests pre- and postdevaluation show that group LiCl-Pellet significantly decreased sign-tracking to the lever following devaluation over sessions. (E) Sign-tracking rates (ppm) during fully rewarded sessions show the same drop following outcome devaluation in Group LiCl-Pellet. (F) Pellet consumption during the pre- and postdevaluation reacquisition sessions. Predevaluation, all animals consumed all pellets, as expected. Postdevaluation, animals in Group LiCl only continued to consume all pellets while animals in group LiCl-Pellet significantly decreased pellet consumption, indicating that outcome devaluation was successful.

Figure 3.

Sign-tracking behavior sensitivity to outcome devaluation extends to single-lever CS preparations. (A) Timeline of experimental procedures: magazine training (Mag), predevaluation extinction session (E1), predevaluation reacquisition session (R1), postdevaluation extinction session (E2), and postdevaluation extinction session (R2). (B) Sign-tracking behavior did not differ between groups on a single-cue sign-tracking protocol over the course of 12 training sessions. Groups increased responding over training days (presses per minute, ppm). (C) Outcome devaluation conducted over the course of five sessions. Sessions 1 and 2, to the left of the dashed line, were conducted in external holding chambers distinct from operant chambers. Sessions 3 and 4 were conducted in operant chambers. Session 5, right of the solid line, was conducted in operant chambers but no lithium chloride was administered following pellet presentation as no pellets were consumed. (D) Sign-tracking rates (ppm) during 5-min extinction tests pre- and postdevaluation show that Group LiCl-Pellet significantly decreased sign-tracking to the lever following devaluation over sessions. (E) Sign-tracking rates (ppm) during fully rewarded sessions show the same drop after outcome devaluation in Group LiCl-Pellet. (F) Pellet consumption during the pre- and postdevaluation reacquisition sessions. Predevaluation, all animals consumed all pellets, as expected. Postdevaluation, animals in Group Saline-Pellet continued to consume all pellets while animals in Group LiCl-Pellet significantly decreased pellet consumption, indicating that outcome devaluation was successful.

Figure 4.

ST sensitivity to outcome devaluation is dependent on outcome devaluation context. (A) Timeline of experimental procedures: magazine training (Mag), postdevaluation extinction session (Ext), and postdevaluation extinction session (Reac). (B) Sign-tracking behavior did not differ between groups on a discriminative sign-tracking protocol over the course of 12 training sessions. Groups readily discriminated between the CS+ and CS− and adjusted responding (presses per minute, ppm) accordingly. (C) Average number of sessions needed to reduce individual rat pellet consumption to less than or equal to one pellet, shown by group. (D) Sign-tracking rates (ppm) during brief 5-min extinction tests on Training Day 12 and postdevaluation shows that Group IN significantly decreased sign-tracking to the lever following devaluation over sessions. (E) Sign-tracking rates (ppm) during fully rewarded sessions show the same drop following outcome devaluation in Group IN. (F) Pellet consumption during the postdevaluation reacquisition session. Animals in Group OUT consumed a greater proportion of pellets than animals in Group IN, indicating that outcome devaluation was more thorough for Group IN.