Sidman instrumental avoidance initially depends on lateral and basal amygdala and is constrained by central amygdala-mediated Pavlovian processes

Abstract

Background: The lateral (LA) and central (CE), but not basal (B), amygdala nuclei are necessary for reactive Pavlovian fear responses such as freezing. The amygdala also plays a key role in the acquisition and expression of active instrumental defensive behaviors, but little is known about the specific roles of amygdala nuclei. Using a Sidman active avoidance (AA) task, we examined the necessity of LA, B, and CE for learning and performance. Pavlovian freezing was simultaneously assessed to examine the contributions of amygdala nuclei to the transition from reactive to active defensive responding.

Methods: Rats received electrolytic lesions of LA, CE, or B before AA training, or following overtraining. Rats that expressed low levels of AA performance during training received bilateral electrolytic lesions to CE to eliminate competing freezing reactions and rescue AA. AA performance and freezing were assessed.

Results: Damage to LA and B, but not CE, impaired the acquisition of AA. Performance of AA became amygdala-independent following overtraining. CE lesions abolished Pavlovian freezing and rescued instrumental AA performance in rats that expressed low levels of avoidance responses and high levels of freezing during training.

Conclusions: Although the acquisition of Pavlovian fear depends on LA and CE, but not B, acquisition of instrumental AA is dependent on LA and B, but not CE. CE-dependent Pavlovian processes that control freezing can constrain avoidance behavior. Performance of well-trained AA becomes independent of all three amygdala nuclei. Thus, it appears that different output pathways of LA mediate reactive and active conditioned defensive responding.

Figure 1

Mean ± SE number of active avoidance (AA) responses across training in rats that recieved pre-training sham surgeries (n = 20) or bilateral electrolytic lesion aimed at lateral amygdala (LA; n = 10), basal amygdala (B; n = 6) or central amygdala (CE; n = 5). Pre-training damage to the LA or B severely impaired acquisition of AA responses. Damage to the CE showed a trend towards facilitation of AA learning during block 1. (*) LA vs Sham = p< 0.05; (+) B vs Sham = p < 0.01.

Figure 2

(a) Mean ± SE number of active avoidance (AA) responses across overtraining in rats that received post-overtraining sham surgeries (n = 10) or bilateral electrolytic lesions aimed at lateral amygdala (LA; n = 4), basal amygdala (B; n = 8) or central amygdala (CE; n = 5). Each block is composed of three training sessions for a total of 15 training sessions. (b) Mean ± SE number of AA responses in the last 2 overtraining sessions compared to the first 2 post-lesion retraining sessions. Post-overtraining lesions had no effect on the number of AA responses during retraining.

Figure 3

(a) Mean ± SE number of active avoidance (AA) responses in good (n = 38) and poor (n = 19) performers across training. Poor performers were animals from the overtraining experiment that did not reach the learning criteria of at least two consecutive sessions of 20 or more AA responses. (b) Mean ± SE percentage freezing at the start of sessions 1, 5, 10 and 15. Freezing levels of good performers decrease as AA training progresses, while freezing remains high in poor performers. (*) session 10: p < 0.01.

Figure 4

(a) Mean ± SE percentage freezing during the first retraining session of poor performers that received sham surgeries (n = 5) or bilateral electrolytic central amygdala (CE) lesions (n = 5). CE damage in poor performers abolished freezing reactions compared to sham. (b) Mean ± SE number of active avoidance (AA) responses for poor performers during the first two retraining sessions. CE-lesioned poor performers showed significantly higher levels of AA responses compared to the sham. In fact, the CE lesion increased AA responses to asymptotic levels of performance by the first retraining session. Dashed line represents the mean for good performers at training day 11, which corresponds to the first retraining session in poor performers.