Elsevier

Addictive Behaviors

Volume 31, Issue 5, May 2006, Pages 833-844
Addictive Behaviors

Working memory in cigarette smokers: Comparison to non-smokers and effects of abstinence

https://doi.org/10.1016/j.addbeh.2005.06.009Get rights and content

Abstract

The present study was designed to examine the effect of cigarette smoking and withdrawal on working memory. Participants included 15 smokers and 22 matched non-smokers. For both groups the N-Back Task (of working memory) was administered in two test blocks on each of two days. On one day, smokers were tested after ≥ 13 h abstinence; on the other day, testing began ≤ 1 h after smoking. Smokers inhaled one cigarette between the blocks on each test day. Results indicated that performance of smokers after ≥ 13 h but not ≤ 1 h abstinence was significantly less accurate than that of non-smokers. A within-subject comparison revealed that in the abstinence session, smokers had significantly longer response latencies (in the 2-back condition) and made more overall errors compared to the satiety session. Smoking between test blocks in the abstinence session did not significantly affect performance although it significantly reduced craving. These findings provide further evidence for a deficit in working memory associated with acute abstinence from smoking, which may contribute to the difficulty of smoking cessation.

Introduction

Working memory is mediated by a system of limited capacity, and it is a component of a wide range of cognitive operations (Baddeley, 1996, Baddeley & Della Salla, 1996). In the simplest case of working memory, information is stored for a few seconds before decaying; in more complex applications, data can be retrieved, manipulated, and associated with other information. Human studies have suggested that chronic smoking, abrupt withdrawal, and acute smoking or nicotine administration can affect performance on tests of working memory, although the results have been inconsistent (Heishman et al., 2002, Heishman et al., 1993, Pritchard & Robinson, 1998, Rezvani & Levin, 2001).

Some research reports have suggested associations between smoking history and impairment on tasks purporting to assess cognitive function. The N-Back Task of working memory (Gevins & Cutillo, 1993), requires the participant to memorize the serial positions of stimuli, presented one at a time, and then, to decide if a given probe was seen 1, 2, or 3 letters prior. Latency for responding to the probe presumably reflects the time needed to mentally scan the items presented. In one study using the N-Back Task, reaction time was shortest in never-smokers, intermediate in ex-smokers, and longest in smokers (Ernst, Heishman, Spurgeon, & London, 2001a). Another study found that smokers, even at smoking satiety, performed more poorly than non-smokers on a recognition memory task in which lists of words were followed by a probe word (Spilich, June, & Renner, 1992). These findings could be interpreted as evidence for a deleterious effect of cigarette smoking. In support of this interpretation, a study of a large cohort found that smokers exhibited greater decline in performance between the ages of 43 and 53 on a word learning task, as compared to non-smokers (Richards, Jarvis, Thompson, & Wadsworth, 2003). Other studies, however, have not demonstrated significant associations between chronic smoking and cognitive decline (Carmelli et al., 1997, Schinka et al., 2002).

Deleterious effects of abrupt initiation of abstinence on working memory, and reversal of such effects by smoking or nicotine administration, have also been observed. For example, within 4 h of initiating smoking abstinence, tobacco-dependent research participants showed increased response latency and poorer accuracy on a digit recall task; their performance returned to baseline levels within 24 h of resuming smoking (Snyder, Davis, & Henningfield, 1989). A similar effect was observed in smokers, whose performance in the a serial recall of letters deteriorated after 12 h of deprivation and normalized after smoking a single cigarette (Blake & Smith, 1997). In another study, abstinent smokers and non-smokers performed a variant of the Sternberg Task, in which a set of items was presented for memorization shortly before the presentation of a single probe item (Grobe, Perkins, Goettler-Good, & Wilson, 1998). The latency for responding to the probe presumably reflected the time needed to scan the memory set being held “on-line.” Nicotine administration by nasal spray improved smokers' performance when distracting stimuli were presented (Grobe et al., 1998). A later study showed that smoking a nicotine-yielding cigarette, but not a de-nicotinized cigarette, shortened reaction times on a Sternberg task (Houlihan, Pritchard, & Robinson, 2001).

Other studies of smoking and/or nicotine manipulations on working memory have yielded results contrasting with those noted above. For example, administration of nicotine gum (4 mg nicotine) did not reduce reaction time or improve accuracy on the N-Back Task in smokers who had abstained for 12 h (Ernst et al., 2001b). Furthermore, in a study in which overnight-abstinent smokers consumed one cigarette whose nicotine content was manipulated, the amount of nicotine delivered was inversely correlated with working memory performance (Williams, 1980). In addition, deficits in spatial working memory were associated with the administration of nicotine nasal spray to abstinent smokers and non-smokers (Park, Knopick, McGurck, & Meltzer, 2000). Summarizing the literature, Pritchard and Robinson (1998) concluded that it “provide[s] no consistent evidence regarding the [acute] effects of smoking/ nicotine on [working memory] capacity” (p. 71).

Complex social and physiological factors contribute to nicotine dependence; and the effects of smoking and of nicotine withdrawal on cognition may contribute to the maintenance and relapse of smoking behavior. The present study therefore aimed to extend knowledge on the interaction of cigarette smoking with working memory performance in humans. We employed a parametric version of the N-Back Task to assess: 1) whether there were differences in working memory between non-smokers and smokers (in abstinence or satiety), 2) whether ≥ 13 h abstinence, compared to relatively brief abstinence (≤ 1 h), resulted in working memory impairments among smokers, and 3) whether smoking one cigarette enhanced the working memory performance of smokers who had been abstaining for ≥ 13 h.

In secondary analyses, we assessed whether self-reported craving was related to working memory performance. In the context of a cognitive test situation, a self-report of craving for a psychoactive entity (e.g., a cigarette) indicates that the research participant is experiencing a cognitive event (Toneatto, 1999), representing intrusive thoughts. Such task-unrelated images or thoughts can capture attention as uncontrolled shifts (Giambra, 1995), and thereby might be expected to interfere with cognitive performance. The effects of withdrawal and smoking history (pack years) also were evaluated.

Section snippets

Participants

Potential participants were recruited from flyers and newspaper ads. They were screened for eligibility during a telephone interview, which included questions about their current use of medications, prior and current use of illicit drugs, medical and psychiatric conditions, and current and previous cigarette usage. Individuals were excluded if they were younger than 18 or older than 55 years of age, or if they reported smoking marijuana more than once per week, drinking more than 10 alcoholic

Participants

Demographic information for the 15 smokers and 22 non-smokers is presented in Table 1. The groups did not differ significantly in age, race, gender or years of education. Smokers did have significantly higher WURS scores (t (33) =  2.14, p = 0.04), suggesting a higher incidence of childhood ADHD in the group. WURS score, therefore, was included in all analyses that included comparisons across groups. The smokers reported a current mean cigarette consumption of 20.4 ± 1.3 (Standard Error) cigarettes

Discussion

This study provides evidence for a working memory deficit associated with acute withdrawal in a sample of smokers with a moderate severity of nicotine dependence. Smokers after ≥ 13 h abstinence, but not in satiety, performed more poorly on the N-Back Task than did non-smokers. More directly, working memory performance by smokers was significantly slower, especially in the 2-back condition, and more prone to errors when the participants had abstained > 13 h as compared to when they were in

Acknowledgments

The following sources of funding contributed to this research:

NIH grants RO1 DA014093.03 (EDL), RO1 DA015059 (ALB), R21 DA 13627 (MSC), and MOIRR 00865; UC Tobacco-Related Disease Research Program 10RT-0091 (EDL) and 11RT-0024 (ALB), Philip Morris USA 01082705 (EDL).

References (32)

  • E. Awh et al.

    Dissociation of storage and rehearsal in verbal working memory: Evidence from positron emission tomography

    Psychological Science

    (1996)
  • A. Baddeley

    The fractionation of working memory

    Proceedings of the National Academy of Sciences of the United States of America

    (1996)
  • A. Baddeley et al.

    Working memory and executive control

    Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences

    (1996)
  • S.C. Baker et al.

    Active representation of shape and spatial location in man

    Cerebral Cortex

    (1996)
  • A.T. Beck et al.

    Assessment of depression: The depression inventory

    Psychological Measurements in Psychopharmacology

    (1974)
  • J. Blake et al.

    Effects of smoking and smoking deprivation on the articulatory loop of working memory

    Human Psychopharmacology

    (1997)
  • Cited by (126)

    • Time-Varying Functional Connectivity Decreases as a Function of Acute Nicotine Abstinence

      2021, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
    • The influence of nicotine metabolic rate on working memory over 6 hours of abstinence from nicotine

      2020, Pharmacology Biochemistry and Behavior
      Citation Excerpt :

      During abstinence from nicotine, as smokers' blood levels of nicotine decrease, difficulty concentrating and decreased alertness are self-reported (Hughes, 2007). In cognitive tests, smokers undergoing nicotine withdrawal show compromised working memory (as measured on the N-back tests) and attentional processes (as measured by the Stroop task) (Mendrek et al., 2006). In Mendrek et al. (2006), significant differences in smokers were found such that when undergoing 13 h of abstinence, reaction times were slower on the 2-back, as compared to when undergoing only 1 h of abstinence.

    View all citing articles on Scopus

    Data was collected at the University of California Los Angeles, Los Angeles, CA, USA.

    1

    Present address: Department of Psychiatry, University of Montreal and Fernand-Seguin Research Center, 7331 Hochelaga, Montreal (QC) H1N 3V2, Canada.

    View full text