Individual variability in behavioral flexibility predicts sign-tracking tendency

Abstract

Sign-tracking rats show heightened sensitivity to food- and drug-associated cues, which serve as strong incentives for driving reward seeking. We hypothesized that this enhanced incentive drive is accompanied by an inflexibility when incentive value changes. To examine this we tested rats in Pavlovian outcome devaluation or second-order conditioning prior to the assessment of sign-tracking tendency. To assess behavioral flexibility we trained rats to associate a light with a food outcome. After the food was devalued by pairing with illness, we measured conditioned responding (CR) to the light during an outcome devaluation probe test. The level of CR during outcome devaluation probe test correlated with the rats' subsequent tracking tendency, with sign-tracking rats failing to suppress CR to the light after outcome devaluation. To assess Pavlovian incentive learning, we trained rats on first-order (CS+, CS-) and second-order (SOCS+, SOCS-) discriminations. After second-order conditioning, we measured CR to the second-order cues during a probe test. Second-order conditioning was observed across all rats regardless of tracking tendency. The behavioral inflexibility of sign-trackers has potential relevance for understanding individual variation in vulnerability to drug addiction.

Keywords: Pavlovian incentive learning; behavioral flexibility; outcome devaluation; second-order conditioning; sign-tracking.

Figure 1

Experiment 1: Phase I–III: Performance during Pavlovian light-food conditioning, conditioned taste aversion and outcome devaluation probe test. (A) Phase I: Light-food conditioning separated by later determined between subjects factor of Pairing: Paired (n = 28) vs. Unpaired (n = 29). Percent time spent in food cup (mean ± SEM) during the last 5 s of the 10 s Pre-CS and CS period of light-food conditioning. (B) Phase II: Pellet consumption during conditioned taste aversion training and post-probe homecage consumption test. Number of pellets consumed (mean ± SEM) in 10 min conditioned taste aversion training sessions (trial 1 and 2) and during post-probe homecage consumption test session (post). (C) Phase III: Overall effect of outcome devaluation during probe test. Percent time spent in food cup (mean ± SEM) during the 10 s light CS and Pre-CS period. Paired (n = 28) vs. Unpaired (n = 29). ^#Different in % time spent in food cup between Paired and Unpaired groups, p = 0.06.

Figure 2

Experiment 1: Phase IV: Performance during lever autoshaping procedure (Sign-tracking screening procedure). Data are mean ± SEM on three different lever-directed (left) and food cup-directed (right) measures. Number of lever and food cup contacts (top row), latency to contact lever or food cup (middle row) and probability of contacting lever or food cup (bottom row).

Figure 3

Experiment 1: Phase IV: Correlation between performance during outcome devaluation probe test with tracking tendency during lever autoshaping. Correlation for Paired (top row) and Unpaired (bottom row) groups between percent time spent in food cup during outcome devaluation probe test (last 5 s of the CS) with composite tracking score determined from lever autoshaping (left) and between percent time spent in food cup during outcome devaluation probe test post-CS period with composite tracking score determined from lever autoshaping (right).

Figure 4

Experiment 1: Phase I–III: Performance during Pavlovian light-food conditioning, conditioned taste aversion and outcome devaluation probe test separated by tracking tendency. (A) Phase I: Light-food conditioning separated by between subjects factor Tracking tendency: sign-tracking (n = 36) vs. non-sign-tracking (n = 21). Percent time spent in food cup (mean ± SEM) during the last 5 s of the 10 s Pre-CS and CS period of light-food conditioning. (B) Phase II: Pellet consumption during conditioned taste aversion training and post-probe homecage consumption test. Number of pellets consumed (mean ± SEM) in 10 min conditioned taste aversion training sessions (trial 1 and 2) and during post-probe homecage consumption test session (post). Paired or Unpaired data is separated by the later determined between subjects factor of tracking tendency. (C) Phase III: Overall effect of outcome devaluation during probe test. Percent time spent in food cup (mean ± SEM) during outcome devaluation probe test separated by tracking tendency during CS (left) and post-CS (right) for Unpaired and Paired groups. ^*Different percent time spent in food cup between Unpaired and Paired groups within tracking tendency, p < 0.05. Paired non-sign-tracking (n = 12); Paired sign-tracking (n = 16) vs. Unpaired non-sign-tracking (n = 9); Unpaired sign-tracking (n = 20). ^#Different in % time spent in food cup between Paired sign-trackers and Paired non-sign-trackers groups, p = 0.05.

Figure 5

Experiment 2: Phase I–II: Performance during Pavlovian first-order light discrimination conditioning and second-order conditioning. (A) Phase I: Performance during Pavlovian first-order light discrimination conditioning. Number of food cup entries (mean ± SEM) during the last 5 s of the 10 s Pre-CS and CS periods of a rewarded light CS+ (blinking or steady, counterbalanced) predictive of food or an unrewarded light CS− (blinking or steady, counterbalanced) predictive of no food. (B–D) Experiment 2: Phase II: Performance during Pavlovian second-order auditory discrimination conditioning. (B) Number of food cup entries (mean ± SEM) during the total 10 s of the Pre-SOCS and SOCS periods for the auditory second-order cues (SOCS+ or SOCS−). (C) Number of food cup entries (mean ± SEM) during the last 5 s of the 10 s Pre-CS and CS for the light first-order cues (FOC compound; CS+ or CS−) when it was presented in compound with the SOCS+ or SOCS−. (D) Number of food cup entries (mean ± SEM) during the last 5 s of the 10 s Pre-CS and CS for the light first-order cues (FOC element; CS+ or CS−) element, “reminder trials,” when these light cues were rewarded or unrewarded, respectively. ^*Different in mean number of food cup entries between SOCS+ vs. SOCS− or CS+ vs. CS−, p < 0.05.

Figure 6

Exp 2: Phase III: Overall performance during second-order probe test. (A) Number of food cup entries (mean ± SEM) during the last 5 s of the 10 s Pre-CS and CS for the light first-order cue (FOC; CS+, or CS−; left panel) and auditory second-order cues (SOC; SOCS+ or SOCS−; right panel). (B) Percent time spent rearing (mean ± SEM) during the first 5 s of the 10 s Pre-CS and CS for the light first-order cues (FOC; CS+ or CS−; left panel) and the total 10 s for the auditory second-order cues (SOC; SOCS+ or SOCS−; right panel). (C) Percent time spent head jerking (mean ± SEM) during the total 10 s Pre-CS and CS for the light first-order cues (FOC; CS+ or CS−; left panel) and the total 10 s for the auditory second-order cues (SOC; SOCS+ or SOCS−; right panel). ^*Different in responding between pre-CS and CS, p < 0.05.

Figure 7

Experiment 2: Phase IV: Performance during lever autoshaping procedure (Sign-tracking screening procedure). Data are mean ± SEM on three different lever-directed (left) and food cup-directed (right) measures. Number of lever and food cup contacts (top row), latency to contact lever or food cup (middle row) and probability of contacting lever or food cup (bottom row).

Figure 8

Experiment 2: Phase IV: Correlation between performance during second-order probe test with tracking tendency during lever autoshaping. Correlations for auditory SOCS+ (top row) and auditory SOCS− (bottom row) using the measure of food cup entries during second-order cue period (last 5 s of the SOCS) with composite tracking score determined from lever autoshaping (left), using the measure of percent time spent rearing during second-order cue period (total 10 s of the SOCS) with composite tracking score determined from lever autoshaping (middle) and using measure of percent time spent head jerking during second-order cue period (total 10 s of the SOCS) with composite tracking score determined from lever autoshaping (right).