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The Journal of Neuroscience, January 21, 2009, 29(3):696-704; doi:10.1523/JNEUROSCI.3758-08.2009

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Behavioral/Systems/Cognitive
The Basolateral Amygdala Is Critical to the Expression of Pavlovian and Instrumental Outcome-Specific Reinforcer Devaluation Effects

Alexander W. Johnson, Michela Gallagher, and Peter C. Holland

Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218

Correspondence should be addressed to Dr. Alexander W. Johnson, Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218. Email: awj{at}jhu.edu

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.

Key words: reward; learning; memory; inactivation; motivation; incentive; limbic

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Received Aug. 8, 2008; revised Oct. 31, 2008; accepted Dec. 4, 2008.

Correspondence should be addressed to Dr. Alexander W. Johnson, Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218. Email: awj{at}jhu.edu

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