Effects of internal and external factors on the budgeting between defensive and non-defensive responses in Aplysia

Abstract

Following exposure to aversive stimuli, organisms budget their behaviors by augmenting defensive responses and reducing/suppressing non-defensive behaviors. This budgeting process must be flexible to accommodate modifications in the animal's internal and/or external state that require the normal balance between defensive and non-defensive behaviors to be adjusted. When exposed to aversive stimuli, the mollusk Aplysia budgets its behaviors by concurrently enhancing defensive withdrawal reflexes (an elementary form of learning known as sensitization) and suppressing feeding. Sensitization and feeding suppression are consistently co-expressed following different training protocols and share common temporal domains, suggesting that they are interlocked. In this study, we attempted to uncouple the co-expression of sensitization and feeding suppression using: 1) manipulation of the animal's motivational state through prolonged food deprivation and 2) extended training with aversive stimuli that induces sensitization lasting for weeks. Both manipulations uncoupled the co-expression of the above behavioral changes. Prolonged food deprivation prevented the expression of sensitization, but not of feeding suppression. Following the extended training, sensitization and feeding suppression were co-expressed only for a limited time (i.e., 24 h), after which feeding returned to baseline levels as sensitization persisted for up to seven days. These findings indicate that sensitization and feeding suppression are not interlocked and that their co-expression can be uncoupled by internal (prolonged food deprivation) and external (extended aversive training) factors. The different strategies, by which the co-expression of sensitization and feeding suppression was altered, provide an example of how budgeting strategies triggered by an identical aversive experience can vary depending on the state of the organism.

Keywords: Aplysia; Behavioral budgeting; Feeding suppression; Food deprivation; Sensitization.

Fig. 1.

In Experiment 1A, prolonged food deprivation prevented the expression of sensitization but not the expression of feeding suppression following single-trial training. The TSWR (A1) and feeding (B1) were measured prior to, and 15 min after training. Sensitization was absent in T-14 animals but was observed in T-2 animals (A2). Conversely, feeding suppression was expressed in both T-14 and T-2 animals (B2). In this and in the following figures, values are expressed as mean ± SEM. Statistical significance was set at p < 0.05.

Fig. 2.

In Experiment 1B, prolonged food deprivation prevented the expression of sensitization but not the expression of feeding suppression following exposure to the four-trial training protocol. TSWR and feeding were tested before and 24h after training (A). Twenty-four hours after training, sensitization was absent in T-14 animals, but was observed in T-2 animals (B). Conversely, feeding suppression was expressed in both T-14 and T-2 animals (C).

Fig. 3.

In Experiment 2, the co-expression of sensitization and feeding suppression was disrupted by an extended training protocol. TSWR and feeding suppression were measured prior to, and 24 h, 72 h and 7 days after extended training (4 trials per day × 4 consecutive days; A). Sensitization (B) and feeding suppression (C) were only co-expressed 24 h after training. Feeding suppression was no longer observed 72 h or 7 days after training (C), whereas sensitization was still expressed at these two time points (B).