Adolescents exhibit behavioral differences from adults during instrumental learning and extinction

Abstract

Adolescence is associated with the development of brain regions linked to cognition and emotion. Such changes are thought to contribute to the behavioral and neuropsychiatric vulnerabilities of this period. We compared adolescent (Postnatal Days 28-42) and adult (Postnatal Day 60+) rats as they performed a simple instrumental task and extinction. Rats were trained to poke into a hole for a food-pellet reinforcer. After six days of training, rats underwent extinction sessions in which the previously rewarded behavior was no longer reinforced. During extinction, we examined the effects of continued presentation of a cue light and food restriction. Adults and adolescents exhibited similar performance during training, although adolescents made more task-irrelevant pokes, consistent with increased exploration. Adults made more premature pokes, which could indicate a more exclusive focus on the task. During extinction, adolescents made more perseverative (previously reinforced) pokes than adults. This behavior was strongly modulated by the combination of motivational factors present (food restriction and cue light), indicating that adolescents were differentially sensitive to them. Furthermore, food restriction induced greater open-field activity in adolescents but not in adults. Thus, as the neural circuitry of motivated behavior develops substantially during adolescence, so too does the behavioral sensitivity to motivational factors. Understanding how such factors differently affect adolescents may shed light on mechanisms that lead to the development of disorders that are manifested during this period.

Figure 1

Adolescent and adult trial performance across training sessions. A) Adolescents perform similar total trials during the first two training sessions. From session 3 onward adults perform more total trials than adolescents (* indicates significant difference between adolescents and adults). B) Within-session average cumulative trial performance over time plus and minus standard error (dashed lines). Sessions 1 and 2 indicate similar or slightly faster performance (steeper slope) by adolescents. The rate of performance is nearly equal during the early portion of sessions 3-6. The drop in trial performance rate after about 5-10 min into those sessions by adolescents contributes to their lower total trials, and may reflect earlier satiety.

Figure 2

Evidence of slightly faster adolescent task acquisition followed by parity of performance. A) The mean latency from trial onset cue to central poke (instrumental response) was shorter in the first training session. During sessions 4-6 this latency became shorter in adults than adolescents. B) Taking only the first 5 minutes of each session, prior to the drop off in within-session cumulative trial performance seen in Figure 1B, we see that adolescent latencies are still shorter in early sessions, but there were no significant latency differences in later sessions. C) There was also no significant age difference in the mean latency from the central poke to the retrieval of the food pellet. (* indicates a significant difference between age groups)

Figure 3

Adolescents and adults perform different behaviors between trials. A) Adults consistently performed more premature (pre-cue) pokes during the ITI than adolescents. In both age groups the number of premature pokes increased, but this increase was more pronounced in adults than adolescents. B) Adolescents consistently performed more task-irrelevant (left- and right-hole) pokes than adults. (* indicates significant age-related differences)

Figure 4

Age-related differences in perseverative (previously reinforced) poking behavior were modulated by the presence of motivational factors. A) When animals remained food restricted and the cue light continued to be presented during extinction, adolescents consistently performed more perseverative pokes than adults. B) When the cue light was omitted but animals were still food restricted, adolescents still perseverated more but this difference was smaller than in A. C) When the animals had ad lib access to food outside of the task and the cue was still presented there were no perseveration differences between adolescents and adults. D) When animals were neither food restricted nor presented the cue, adults performed fewer perseverative pokes. Adolescents in this condition were more similar in their perseveration to their counterparts exposed to a single motivational factor as in B and C. (* indicates significant age-related differences)

Figure 5

Interaction plots demonstrating differences between adolescents and adults in their sensitivities to the presence of motivational factors in different combinations collapsed across extinction sessions. A) Among food-restricted animals a significant age × cue presence interaction was observed. Adolescents perseverated more than food-restricted adults generally, but importantly the presence of the cue had a stronger activating effect on adolescents than adults. B) There was no age × cue presence interaction in ad lib animals. C) A significant age × food-restriction status interaction was observed for animals presented the cue. Among these animals only the food-restricted adolescents perseverated more than adults. C) When animals were not presented the cue there was no age × food-restriction status interaction. E) In adolescents, the combination of both motivational factors interacted to further increase in perseveration. A single or no motivational factor led to similar lower levels. B) Unlike adolescents, in adults the combination of motivational factors did not interact synergistically to further increase perseverative pokes. (^† indicates significant interactions)

Figure 6

Task-irrelevant poking behavior during extinction. A) Adolescents consistently performed more task-irrelevant pokes during extinction. B) A main effect of food-restriction status was observed, although only ad lib adults performed significantly fewer task-irrelevant pokes. (^‡ indicates a significant difference in task-irrelevant pokes as a function of food-restriction status within an age group)

Figure 7

Adolescents exhibited more open field activity which was modulated by food-restriction status. A) Adolescents performed more total grid entries than adults. This behavior was increased in food-restricted adolescents. There was no significant difference in total grid entries as a function of food-restriction in adult rats. B) Adolescents entered the central grid area more than adults and again food restriction increased this behavior in the younger animals. Adult central-grid entries were unaffected by food-restriction status. (* indicates a significant age-related difference; ^‡ indicates a significant difference as a function of food-restriction status within an age group)