The glucocorticoid response in a free-living bird predicts whether long-lasting memories fade or strengthen with time

Abstract

For decades, scientists have used threat conditioning (traditionally termed ‘fear conditioning’) to study the link between glucocorticoids and the consolidation of long-term memories (i.e. memories that last hours to weeks) in model organisms in the laboratory. We assessed this relationship in a free-living species, and examined a possible relationship between glucocorticoids and the retention of long-lasting memories (i.e. memories that last months to a lifetime). We developed a novel threat-conditioning protocol by which free-living Florida scrub-jays, Aphelocoma coerulescens, were either chased by a novel predator or exposed to a control. We measured flight initiation distance (FID) 48 h, 11 months and 2 years after conditioning or control exposures, and compared these measures to levels of stress-induced glucocorticoids. Conditioned subjects maintained significantly longer FIDs for at least 2 years. Furthermore, the long-term memory consolidation of conditioned subjects positively correlated with their stress-induced glucocorticoid response, similar to results from laboratory studies. Surprisingly, individuals with a moderate stress response exhibited an exaggerated defence response (i.e. FIDs increased) at 11 months and 2 years post-conditioning, whereas low and high stress responders exhibited memory decay or extinction (i.e. FIDs decreased). We speculate that the recently discovered processes of memory reconsolidation and system consolidation may help explain why some Florida scrub-jays exhibit more fearful-like behaviour with time.