Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding

https://doi.org/10.1016/S1074-7427(02)00036-9Get rights and content

Abstract

Abundant evidence indicates that endogenous stress hormones like epinephrine and cortisol modulate memory consolidation in animals. Despite this evidence, there has been no demonstration that endogenous stress hormones modulate memory consolidation in humans. In the present study, healthy subjects viewed a series of 21 slides, and immediately after received an intravenous infusion of either saline or epinephrine (40 or 80 ng/kg/min). Memory for the first three (primacy) and last three (recency) slides viewed was assessed with an incidental free recall test one week later. Epinephrine dose-dependently increased memory for the primacy slides, but did not affect memory of the recency slides. A subsequent experiment involving new subjects revealed significantly higher electrodermal responses to the primacy compared with recency slides. These findings support the view (Gold & McGaugh, 1975) that endogenous stress hormones modulate memory consolidation for experiences that induce their release. Additionally, they suggest that in humans these hormones may interact with the degree of arousal at initial encoding of information to modulate memory consolidation processes for that information.

Introduction

Considerable evidence suggests that adrenergic hormones modulate the consolidation of long-term memory for experiences that induce their release. For example, post-training injection of adrenergic drugs or hormones enhances memory consolidation in many species (Cahill & McGaugh, 1998; Cahill, Prins, Weber, & McGaugh, 1994; Gold & van Buskirk, 1975; McGaugh, 2000; McGaugh, Cahill, & Roozendaal, 1996; Soetens, Casaer, D’Hooge, & Hueting, 1995). Despite this evidence, no demonstrations exist of enhanced memory consolidation in humans produced by adrenergic hormones, although enhanced consolidation in humans has been reported with post-learning administration of amphetamine (Soetens et al., 1995) glucose (Manning, Parsons, & Gold, 1992), and yohimbine (Southwick et al., 2002). The hypothesis that endogenous adrenergic hormones compose a necessary part of an endogenous memory-modulating system for emotionally arousing events in humans (Cahill & McGaugh, 1998) requires that, in appropriate conditions, these hormones be shown to enhance human long-term memory consolidation.

In this study, healthy humans received an intravenous infusion of epinephrine (EPI) after viewing a series of standardized slides. On the basis of a straightforward ‘time dependency’ view of memory consolidation (McGaugh, 1966), we predicted that EPI would most likely enhance memory for the slides viewed most recently before the infusion (recency effect). Other evidence suggests that drug-induced memory enhancement in humans can be restricted to the primacy portion of a series of items (Crow, 1979; Messier, Pierre, Desrochers, & Gravel, 1998). Therefore, we also examined the influence of EPI on retention of the initial slides viewed (primacy effect).

Section snippets

Materials and methods

Healthy volunteers (mean age (±SEM)=21.9±0.7 years, 22 male, 20 female). viewed a series of 21 standardized slides (Lang, Bradley, & Cuthbert, 1999) while seated comfortably before a viewing screen. Prior to slide viewing, each subject received an intravenous line in their left arm, and electrodes for continuous monitoring of heart rate (MP100 recording system, Biopac Instruments, Santa Barbara, CA) and pressure cuff on their right arm for blood pressure monitoring. The time between insertion

Results

Post-learning epinephrine administration significantly enhanced memory for the primacy slides (Fig. 1). A one-factor ANOVA of recall scores revealed a significant effect of drug condition [F(2,39)=3.74, p<.05]. Post-hoc t tests comparisons revealed a significant difference that subjects in the EPI 80 group recalled significantly more of the primacy slides that did subjects in the saline group [t(30)=−2.78,p=.009]. ANOVA of recall scores for the recency portion revealed no significant difference

Discussion

These findings support two primary conclusions. First, consistent with prior animal research, adrenergic hormones can produce retrograde enhancement of long-term memory in humans. Because epinephrine was administered after learning, its enhancing effect on memory cannot be attributed to actions on attentional, emotional, perceptual, or encoding processes during slide presentation. The findings thus provide new support for the hypothesis that adrenergic hormones, released by emotionally

Acknowledgments

Supported by NIMH Grant MH-57508 to L.C.

References (24)

  • I.M. Colrain et al.

    Effects of post-learning smoking on memory consolidation

    Psychopharmacology (Berlin)

    (1992)
  • T. Crow
  • Cited by (379)

    View all citing articles on Scopus
    View full text