The basolateral amygdala is necessary for negative prediction errors to enhance cue salience, but not to produce conditioned inhibition

• Published in: The European journal of neuroscience 2014-11, Vol.40 (9), p.3328-3337
• Main Authors: Esber, Guillem R., Holland, Peter C.
• Format: Article
• Language: English
• Subjects: Animals; associative learning; Attention - physiology; basolateral amygdala; Basolateral Nuclear Complex - physiology; Biological and medical sciences; conditioned inhibition; Conditioning, Classical - physiology; Cues; Fundamental and applied biological sciences. Psychology; Inhibition (Psychology); Male; prediction error; Proto-Oncogene Proteins c-fos - metabolism; Rats, Long-Evans; salience; unblocking; Vertebrates: nervous system and sense organs
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.12695

Behavioral evidence shows that prediction errors (PEs) not only drive associative learning, but also enhance the salience of predictive cues, making them better able to capture attention when they are next encountered. Research from our laboratory suggests that this latter consequence of PEs depends on a neural circuit that includes the amygdala. Lesions of the basolateral complex of the amygdala (BLA), for instance, selectively disrupt enhancements in cue processing that are normally induced by positive PEs without compromising simple excitatory learning. This result is consistent with electrophysiological evidence showing that BLA neurons track positive PEs. Interestingly, the same neurons also seem to track negative PEs, suggesting the possibility that the BLA might also use these errors to drive enhancements in cue processing. Here, we examined the role of the BLA in the processing (Experiment 1) and utilization (Experiment 2) of negative PEs in increasing cue salience in an unblocking procedure. Using FOS expression as an index of neural activity, Experiment 1 confirmed that BLA neurons track negative PEs with reinforcement downshifts. This tracking was evident both when these errors were generated by decreasing the concentration of a sucrose reinforcer (which encourages the development of conditioned inhibition) and when they were generated by decreasing the number of sucrose reinforcers (which encourages excitatory learning – unblocking – and allows the detection of enhancements in cue processing). Experiment 2 demonstrated that BLA lesions abolished enhancements in cue processing while sparing inhibitory learning. These results suggest a general role of the BLA in utilizing PEs, whatever their sign, for boosting cue processing. Negative reward prediction errors produced by downshifts in either number or concentration of a sucrose reward enhanced FOS expression in the basolateral amygdala (BLA) compared to a blocking control treatment. Only downshifts in reinforcer number produced excitatory conditioning to an added cue (unblocking); that unblocking was absent in rats with BLA lesions. Downshifts in reinforcer number instead yielded conditioned inhibition, which was not affected by BLA lesions.