Age and sex differences in reward behavior in adolescent and adult rats

Abstract

Compared to adults, adolescents are at heightened risk for drug abuse and dependence. One of the factors contributing to this vulnerability may be age-dependent differences in reward processing, with adolescents approaching reward through stimulus-directed, rather than goal-directed, processes. However, the empirical evidence for this in rodent models of adolescence, particularly those that investigate both sexes, is limited. To address this, male and female rats that were adolescents (P30) or adults (P98) at the start of the experiment were trained in a Pavlovian approach (PA) task and were subsequently tested for the effects of reward devaluation, extinction, and re-acquisition. We found significant interactions between age and sex: females had enhanced acquisition of PA and poorer extinction, relative to males, while adolescents and females were less sensitive to reward devaluation than male adults. These results suggest that females and adolescents exhibit reward behavior that is more stimulus-directed, rather than goal-directed.

Keywords: Pavlovian approach; adolescent; extinction; learning; rat; reacquisition; reward devaluation; reward processing; sex.

Figure 1

Total trough entries during magazine training sessions for male (M) and female (F) adolescent and adult rats (n = 10–12/group). ** p < 0.01 vs. adolescent females

Figure 2

Approach behavior during the first eight conditioning sessions (n = 10–12/group). Panel A shows CS⁺ approach, panel B shows CS− approach. The approach score was calculated as a difference score: trough entries during the 8 10-s CS trials - trough entries during the 8 10-s periods preceding each CS trial. * p < 0.05, ** p < 0.01 and *** p < 0.001, vs. adolescent females; ^@ p < 0.05 and ^@@ p < 0.01 vs. adult males

Figure 3

Approach behavior following reward devaluation (n = 10–12/group). Panel A shows consumption of 20% sucrose solution, relative to bodyweight, during the 60 min free access period. Panel B shows CS⁺ approach during the 8^th conditioning session and the reward devaluation session. Panel C shows the change in CS⁺ approach following devaluation, calculated as a difference score: devaluation session CS⁺ approach – conditioning session 8 CS⁺ approach. ⁺ p < 0.05, ⁺⁺ p < 0.01 and ⁺⁺⁺ p < 0.001, vs. adolescent males; ^@ p < 0.05 and ^@@ p < 0.01, vs. adult males

Figure 4

Extinction and reacquisition (n = 10–12 rats/group). Panel A shows the CS⁺ approach for the two conditioning sessions prior to extinction, as well as the CS⁺ approach during each day (average of morning and evening sessions) of extinction. Panel B shows CS⁺ approach during reacquisition. * p < 0.05 and *** p < 0.001, vs. adolescent females; ^# p < 0.05 vs. adult females; ⁺ p < 0.05 vs. adolescent males; ^@@@ p < 0.001, vs. adult males