Different Roles for Amygdala Central Nucleus and Substantia Innominata in the Surprise-Induced Enhancement of Learning

Abstract

Within most modern learning theories, the discrepancy between expected and obtained outcomes ("prediction error" or "surprise") is a critical determinant of the acquisition of learned associations. The results of studies from many laboratories show that the surprising omission of an expected event may enhance attention to stimuli that remain present, such that subsequent learning about those stimuli is enhanced. A series of reports from our laboratories demonstrated that these surprise-induced enhancements of stimulus associability depend on circuitry that includes the amygdala central nucleus (CeA), the cholinergic neurons in the sublenticular substantia innominata/nucleus basalis magnocellularis (SI/nBM), as well as certain cortical projections of these latter neurons. In this study, we found very different roles for CeA and SI/nBM in surprise-induced enhancements of stimulus associability. In four experiments that used transient inactivation techniques, we found that surprise-induced enhancement of subsequent learning about a stimulus depended on intact CeA function at the time of surprise but not when more rapid learning was subsequently expressed. In contrast, normal SI/nBM function was critical to the expression of enhanced learning but was not necessary when surprise was induced. These data suggest that these two components of the so-called "extended amygdala" serve distinct roles in the encoding and retrieval of information used in modulating attention to stimuli in associative learning. Additional circuitry linking these brain regions may also be important in the maintenance of that information.