Setting the occasion for adolescent inhibitory control

Abstract

During adolescence, individuals experience a broad range of dynamic environments as they strive to establish independence. Learning to respond appropriately in both new and previously encountered environments requires that an individual identify and learn the meaning of cues indicating that a behavior is appropriate, or alternatively, that it should be altered or inhibited. Although the ability to regulate goal-directed behavior continues to develop across adolescence, the specific circumstances under which adolescents experience difficulty with inhibitory control remain unclear. Here we review recent findings in our laboratory that address how adolescents learn to proactively inhibit a response. Much of our research has utilized a negative occasion setting paradigm, in which one cue (a feature) gates the meaning of a second cue (a target). The feature provides information that resolves the ambiguity of the target and indicates the appropriate behavioral response to the target. As such, we have been able to determine how adolescents learn about ambiguous stimuli, such as those whose meaning changes in accordance with other features of the surrounding environment. We consider why adolescents in particular exhibit difficulty in negative occasion setting compared to either pre-adolescents or adults. In addition, we review findings indicating that a balance in neural activity between orbitofrontal cortex and nucleus accumbens is necessary to support normal negative occasion setting. Finally, we consider aspects of associative learning that may contribute to adolescent inhibitory control, as well as provide insight into adolescent behavior as a whole.

Keywords: Adolescence; Inhibition; Learning.

Figure 1

A) Illustration of the two types of training trials used in our standard negative occasion setting procedure with rats. The feature (light) and target (tone) are each presented for 5 sec and the interval between them on non-reinforced trials is also 5 sec. On reinforced trials, food is delivered immediately after the tone is terminated. B) Model of the associations that are thought to be formed during negative occasion setting [40]. Red and green lines indicate inhibitory and excitatory relationships in the behavioral procedure, respectively (US = unconditioned stimulus). The feature stimulus acts to gate, or ‘set the occasion’ for the meaning of the target stimulus and indicates that a response should be withheld during the subsequent presentation of the target.

Figure 2

A) Number of daily training sessions required by adolescent (started training on PND 35) and adult (PND 70) rats to consistently exhibit significantly more responding to the target on reinforced versus non-reinforced trials (adapted from [19]). Criterion was 3 consecutive sessions in which the group mean difference in responding during reinforced and non-reinforced trials was significantly greater than zero (i.e., Z-score of at least 2.325, p<0.01). B) Results of an experiment to test whether adolescent rats were impaired in acquiring the contingencies during negative occasion setting, or in expressing that learning. Rats in the ‘paired pre-train’ group received six sessions of negative occasion setting training starting on PND 35. Rats in the ‘unpaired pre-train’ group were treated similarly but the stimuli were presented randomly and in an unpaired fashion. Both groups remained in their home cages for 9 days after the pre-training sessions. Then when they were 50 days only, they resumed negative occasion setting training. The no pre-train group did not receive any pre-training and had its first experience with the negative occasion setting procedures starting on PND 50.

Figure 3

Effects of counterconditioning (light paired with food) on conditioned responding to the target when rats were returned to the negative occasion setting procedures (NOS test). Percent difference reflects the amount of responding to the target on reinforced trials divided by responding to the target on non-reinforced trials, multiplied by 100. Thus, a value of 100% (dotted line) indicates that responding during reinforced trials was the same as responding on non-reinforced trials. Adult rats exhibited little change in responding to the target during the NOS test session compared to the end of NOS training. In contrast, counterconditioning reduced responding to the target in adolescent rats.

Figure 4

‘Imbalance model’ of adolescent brain development [64]. NAC = nucleus accumbens, PFC=prefrontal cortex. Dotted line refers to activity levels in adults. During adulthood, both NAC and PFC have reached functional maturity and their activity levels are in balance. Similarly, during pre-adolescence, both regions are immature and activity levels are lower than in adults, but still balanced in relationship to each other. In contrast, there is an imbalance that arises in adolescents because maturation of PFC lags behind that of NAC, and NAC activity is increased.

Figure 5

Number of daily training sessions required to exhibit negative occasion setting by rats that started training prior to the onset of adolescence (PND 30), during adolescence (PND 35, 40), late adolescence/early adulthood (PND 50), and full adulthood (PND 70). Adapted from [20].

Figure 6

Number of daily training sessions required to exhibit negative occasion setting in adult rats with artificially reduced levels of activity in orbitofrontal cortex (OFC), or increased activity in NAC, or a combination of both manipulations. Adapted from [83].