The basolateral amygdala is critical to the expression of pavlovian and instrumental outcome-specific reinforcer devaluation effects

Abstract

Considerable evidence implicates the basolateral amygdala (BLA) in the formation of outcome representations that link cues to the incentive properties of reinforcers. Animals with BLA damage show impaired performance in reinforcer devaluation tasks, in which the value of the food reinforcer is reduced by satiation or food-toxin pairings after the completion of cue or response training. Although intact animals spontaneously reduce their conditioned responding after such reinforcer devaluation procedures, animals with BLA lesions made before training typically do not, as evidenced across a range of species, training contingencies, and devaluation procedures. In contrast, the role of the BLA in devaluation task performance once such outcome representations are established is unclear. Whereas Pickens et al. (2003) found normal devaluation performance in rats when BLA lesions were made after pavlovian light-food pairings but before devaluation by food-toxin pairings, Ostlund and Balleine (2008) found impaired devaluation performance when BLA lesions were made after instrumental training with multiple instrumental responses and food reinforcers but before devaluation of one reinforcer by selective satiation. Those studies differed in their use of pavlovian or operant training contingencies, single or multiple reinforcers, and associative or motivational devaluation procedures. Here we found that, when multiple reinforcers were used, posttraining BLA lesions disrupted the expression of devaluation performance in rats, using either pavlovian or instrumental training procedures and either conditioned taste aversion or satiation devaluation procedures. Thus, BLA apparently plays a critical role in maintaining or using sensory associations of reinforcer value when multiple outcomes must be coded but not under single-outcome conditions.

Figure 1.

BLA lesion histology. Photomicrographs of coronal sections of the amygdala from the brains of representative sham-lesioned (a) and BLA-lesioned (b) rats. c, Extents of minimum, maximum, and representative BLA lesions at various distances posterior to bregma.

Figure 2.

Experiment 1 behavioral results. Mean lever presses per minute during instrumental training for BLA-lesioned (a) and sham-lesioned (b) rats for the response in training that delivered the outcome subsequently devalued by sensory-specific satiety (devalued response; filled symbols) and for the response that subsequently remained valued (non-devalued response; open symbols). Mean lever presses per minute during choice extinction test for BLA-lesioned (c) and sham-lesioned (d) rats for the response associated with the devalued (filled symbols) and non-devalued (open symbols) outcome. Error bars indicate SEM.

Figure 3.

Experiment 2 behavioral results. Mean lever presses per minute during instrumental training for BLA-lesioned (a) and sham-lesioned (b) rats for the response in training that delivered the outcome subsequently devalued by conditioned taste aversion (devalued response; filled symbols) and for the response that subsequently remained valued (non-devalued response; open symbols). Mean lever presses per minute during choice extinction test for BLA-lesioned (c) and sham-lesioned (d) rats for the response associated with the devalued (filled symbols) and non-devalued (open symbols) outcome. Error bars indicate SEM.

Figure 4.

Experiment 3 behavioral results. Percentages of time spent in the food cup during pavlovian training of the cue paired with the subsequently devalued outcome (filled symbols) and the cue paired with the outcome that subsequently remained valued (open symbols) in BLA-lesioned (a) and sham-lesioned (b) rats. c, Percentages of time spent in food cup during pavlovian extinction test in BLA- and sham-lesioned rats for the cue associated with the devalued outcome (filled bars) and the cue associated with the non-devalued outcome (open bars). d, Consumption (in milliliters) of devalued (filled bars) and non-devalued (open bars) reward during reinforcer choice test for BLA- and sham-lesioned rats.

Figure 5.

Experiment 4 behavioral results. Percentages of time spent in the food cup during pavlovian training of the cue paired with the subsequently devalued outcome (filled symbols) and the cue paired with the outcome that subsequently remained valued (open symbols) in BLA-lesioned (a) and sham-lesioned (b) rats. c, Percentages of time spent in food cup during pavlovian extinction test in BLA- and sham-lesioned rats for the cue associated with the devalued outcome (filled bars) and the cue associated with the non-devalued outcome (open bars). d, Consumption (in milliliters) of devalued (filled bars) and non-devalued reward (open bars) during reinforcer choice test for BLA- and sham-lesioned rats