Rats exposed to intermittent ethanol during late adolescence exhibit enhanced habitual behavior following reward devaluation

Abstract

The brain undergoes substantial maturation during adolescence, and repeated exposure to ethanol at this time has been shown to result in long-lasting behavioral and neural consequences. During the broad period of adolescence, different neuronal populations and circuits are refined between early and late adolescence, suggesting the possibility that ethanol exposure at these differing times may lead to differential outcomes. The goal of the current study was to evaluate the impact of adolescent intermittent ethanol (AIE) during early and late adolescence on the formation of goal-directed and habitual behavior in adulthood. Male and female Sprague-Dawley rats were exposed to ethanol via intragastric gavage (4.0 g/kg, 25% v/v) every other day from postnatal day (P) 25-45 or P45-65, considered early and late adolescence, respectively. In adulthood (~P70 early or ~ P90 late), rats were gradually food-restricted and began operant training on a fixed ratio 1 schedule. Rats were then transitioned onto random interval schedules and eventually underwent a sensory-specific satiation procedure as a model of reward devaluation. Few differences as a result of adolescent ethanol exposure were found during instrumental training. Following reward devaluation, rats exposed to water and ethanol during early adolescence exhibited reductions in lever pressing, suggestive of a goal-directed response pattern. In contrast, late AIE males and females demonstrated persistent responding following both devalued and non-devalued trials, findings representative of a habitual behavior pattern. The shifts from goal-directed to habitual behavior noted only following late AIE contribute to the growing literature identifying specific behavioral consequences as a result of ethanol exposure during distinct developmental periods within adolescence. More work is needed to determine whether the greater habit formation following late AIE is also associated with elevated habitual ethanol consumption.

Keywords: Adolescence; Goal-Directed; Habit formation; Intermittent ethanol exposure; Sex differences.

Figure 1.

Lever presses per minute made during operant training. All groups increased lever pressing across FR1 training. For males, a decrease in lever pressing across RI training was evident, regardless of age of exposure and exposure condition (A). In addition, early-exposed males tended to make more lever presses per minute than late-exposed males. In contrast, no differences were seen for females (B). * indicates main effect of test day and # indicates main effect of age of exposure.

Figure 2.

The amount of sucrose pellets consumed (g/kg) during the 1-hour free access periods prior to extinction testing. All groups (A–B) had increased consumption of pellets in the devalued condition in comparison to the non-devalued condition. Early-exposed males also had greater sucrose pellet consumption compared with late adolescent-exposed males. ** (p < 0.01) and **** (p < 0.0001) indicate main effect of devaluation and # indicates main effect of age of exposure, p < 0.05.

Figure 3.

Normalized responding made during the 10-minute extinction trial following the sensory-specific satiation procedure. For both sexes, early and late adolescent water- and ethanol-exposed animals (A and C) had reduced lever press responses following devaluation. When assessing the devaluation index (B and D), late AIE males and females did not display different response patterns between devalued and non-devalued conditions. *** (p < 0.001) and **** (p < 0.0001) indicate main effect of devaluation and # indicates main effect of age of exposure, p < 0.05 (A and C) and devaluation index significantly different from 0 indicated by * (p < 0.05) and ** (p < 0.01, B and D).

Figure 4.

Post-consumption test to ensure the effectiveness of the sensory-specific satiation procedure. All conditions had greater intake of the sucrose pellets that were not devalued prior to testing (A and B). Early adolescent-exposed males also consumed more than late adolescent-exposed males. ** (p < 0.01) indicates main effect of devaluation and # indicates main effect of age of exposure, p < 0.05.