Neural correlates of variations in event processing in the basolateral and central nuclei of the amygdala

Abstract

Throughout history, psychologists have sought to understand how neutral stimuli in the environment gain emotional significance after pairing with biologically relevant consequences. The amygdala is a brain region that has been repeatedly implicated in associative learning, and is widely thought to be the initial site where incoming sensory information gains emotional significance. Learning theorists suggest that the formation of such associations may be driven by variations in the processing of events which are encountered in the environment. Models of attention-driven learning, such as that of Pearce and Hall (1980), posit that unexpected events require more attention to drive learning than events which are reliably predicted. Recent findings indicate that certain amygdalar nuclei may be involved in enhancing attention for unexpected events. In particular, the central and basolateral nuclei of the amygdala have been independently implicated in serving a role in attentional function. However, we have a remarkably limited understanding of the neural representation of events which enhance attention, particularly regarding how amygdalar nuclei may signal unexpected changes in reinforcer value. Here, we use a task which violates rat's expectations by suddenly increasing or decreasing reward value, while we record from or reversibly inactivate the basolateral or central nucleus of the amygdala. We found that neurons in both nuclei were sensitive to changes in reinforcer value, firing more strongly to unexpected events than to those same outcomes when they were learned. The observed changes in neural activity correlated with subsequently expressed behavioral measures of attention. Importantly, while neurons in the basolateral amygdala encoded changes to reinforcer value generally for both upshifts and downshifts in reward value, neurons in the central nucleus were selectively sensitive to unexpected downshifts in reward value. Further, inactivation of either nucleus disrupted attention-driven behaviors, and in the case of basolateral inactivation, retarded learning in the task. Such findings support a role for the basolateral and central nuclei of the amygdala in signaling variations in event processing, activity which has profound theoretical implications for processing in downstream reward circuitry and for the subsequent expression of learning.