Amphetamine Fails to Alter Cued Recollection of Emotional Images: Study of Encoding, Retrieval, and State-Dependency

Jessica Weafer,David A Gallo,Harriet De Wit,Manabu Sakakibara

doi:10.1371/journal.pone.0090423

Abstract

Stimulant drugs facilitate both encoding and retrieval of salient information in laboratory animals, but less is known about their effects on memory for emotionally salient visual images in humans. The current study investigated dextroamphetamine (AMP) effects on memory for emotional pictures in healthy humans, by administering the drug only at encoding, only at retrieval, or at both encoding and retrieval. During the encoding session, all participants viewed standardized positive, neutral, and negative pictures from the International Affective Picture System (IAPS). 48 hours later they attended a retrieval session testing their cued recollection of these stimuli. Participants were randomly assigned to one of four conditions (N = 20 each): condition AP (20 mg AMP at encoding and placebo (PL) at retrieval); condition PA (PL at encoding and AMP at retrieval); condition AA (AMP at encoding and retrieval); or condition PP (PL at encoding and retrieval). Amphetamine produced its expected effects on physiological and subjective measures, and negative pictures were recollected more frequently than neutral pictures. However, contrary to hypotheses, AMP did not affect recollection for positive, negative, or neutral stimuli, whether it was administered at encoding, retrieval, or at both encoding and retrieval. Moreover, recollection accuracy was not state-dependent. Considered in light of other recent drug studies in humans, this study highlights the sensitivity of drug effects to memory testing conditions and suggests future strategies for translating preclinical findings to human behavioral laboratories.

Highlights

Drug addiction is thought to be a disorder of learning and memory [1,2]
We focused our analyses on the Elation and Vigor scales, as these represent the typical positive, rewarding effects of amphetamine (e.g., [33,34,35])
This study examined the effect of assessed the effects of dextroamphetamine (AMP) and drug statedependency on memory for emotional material in healthy humans

Summary

Introduction

Drug addiction is thought to be a disorder of learning and memory [1,2]. This hypothesis originated in part from evidence that drugs of abuse act directly on emotional memory systems that guide reward-related learning [3,4]. The effects of stimulant drugs on learning and memory for incentive stimuli have been studied in animal models, but less is known about their effects on memory for emotionally salient material in humans Stimulants such as nicotine and amphetamine facilitate both encoding and retrieval of salient information in laboratory animals. AMP administered at encoding enhanced recognition memory accuracy relative to placebo, especially for emotional stimuli (both positive and negative), providing the first evidence that acute stimulant administration enhances encoding of emotionally salient material. An additional methodological difference between this and our previous studies was our decision to use a between-subjects design, in which we administered the drug only at encoding, only at retrieval, or at both encoding and retrieval This design avoids any potentially confounding effects of task order, allowing for the clearest test of state-dependency. We predicted that memory would be greater when encoding and retrieval occurred in the same state (i.e., AMP-AMP or PL-PL) compared to different states (i.e., AMP-PL or PL-AMP)

Methods

Results

Discussion