Research reportComparing the benefits of caffeine, naps and placebo on verbal, motor and perceptual memory
Introduction
Caffeine, the world's most widely consumed stimulant [1], is an active ingredient in coffee, tea, chocolate, sodas, and energy drinks (the fastest growing sector of the American beverage industry) [2]. Modern times have led to an increase in daily, often multiple doses of caffeine, a rise in the coffee business, and the addition of caffeine to common beverages such as soda, bottled water, and even chewing gum. Based on the available product usage and food consumption data, Barone and Roberts [3] estimated the mean daily intake was 4 mg/kg body weight (approximately 280 mg for a 155 pound person; 16 ounces of Starbucks coffee contains 372 mg). For the 90th percentile of caffeine users, intakes approximated 5–7 mg/kg body weight (approximately 300–500 mg).
This increasingly common use of caffeine in our society coincides with an increasingly common trend of individuals obtaining insufficient sleep on a regular basis. While it is difficult to ascertain the exact number of individuals who use caffeine as a substitute for sleep in society, the 2005–2007 National Sleep Foundation's annual Sleep in America polls strongly suggest that Americans regularly consume caffeine as a substitute for sleep and/or as a result of insufficient sleep [4], [5], [6]. These polls report consistent associations between low quantity or quality of sleep, decreased daytime functioning, and increased daytime caffeine consumption.
A number of studies have examined the benefits of daytime caffeine consumption in non-experimentally sleep-deprived individuals [7], [8], [9], [10], [11], [12], [13], [14], [15], [16], [17], [18], [19]. The performance tasks used in these studies measure reaction time and motor speed, speed of information processing, vigilance and attention, immediate and delayed verbal memory, as well as mood and alertness (for review see [10], [18]. Generally, caffeine enhances mood and alertness [8], [14], vigilance and attention [8], [9], speed of information processing [14], [19], reaction time and motor speed [8], [9], [14], [19]. One study found 200 and 300 mg of caffeine benefited visual vigilance, choice reaction time, repeated acquisition, and self-reported fatigue and sleepiness, but did not improve marksmanship, a task that requires fine motor coordination and steadiness [16], [17]. Dimpfel et al. measured the effects of placebo, 200 and 400 mg of caffeine on human electroencephalogram (EEG) patterns at rest and during mental concentration tests. In addition to the finding that the effects of caffeine can be quantified with EEG spectral densities, they also found that subjects achieved the best results on concentration tests when given 200 mg of caffeine. In fact, subjects given 400 mg tested below subjects in the placebo condition. Other studies have found similar improvements on cognitive tasks with as little as 70 mg of caffeine administration compared to placebo [20].
While these studies show caffeine can enhance wakefulness and performance on attention and concentration tasks, little agreement can be found in the literature on caffeine and memory [7], [19], [21]. In their review, Nehlig et al. [10] write “In man, memory per se is not improved but response tends to be quicker and keener [with caffeine]”. An alternative explanation for the negative findings is that only a limited number of memory processes have been examined. A thorough examination of the effect of caffeine across a wide range of memory processes has not been completed. Thus, it is still an open question whether caffeine improves learning and memory [1], [12], either more generally or in specific memory domains.
Naps, in contrast to caffeine, have been shown to enhance not only alertness and attention, but also some forms of memory consolidation. In particular, naps (daytime sleep between 5 and 90 min) appear to improve performance on non-medio-temporal lobe dependent, procedural skills [22], [23], [24], [25]. Mednick et al. reported that a mid-day nap can also reverse perceptual deterioration that builds with repeated within-day testing [22]. They further showed that naps with SWS and REM produced improvements in performance equivalent to that of a full night of sleep, whereas naps with only SWS restored deteriorated performance to baseline levels [23]. Walker and coworkers have demonstrated that naps improve procedural motor skill learning to the same degree as a full night of sleep, and that improvement on this task was correlated with Stage 2 and sleep spindle activity [25], [26]. Tucker compared naps with non-REM sleep to a no-nap condition on a procedural memory task and a declarative, verbal-paired-associates task. They found that the non-REM naps produced improved performance in the declarative, but not the procedural task [27]. This is evidence that non-REM in naps can produce similar declarative memory improvements as nocturnal non-REM sleep [28].
Prior studies of performance during nightshift work have directly compared caffeine and napping in on a variety of tasks [29], [30]. For example, recently, Sagaspe et al. compared the effects of a single 200 mg dose of caffeine to a 30 min nap and placebo on nocturnal driving in young and middle-aged participants. They found that both interventions significantly improved performance in both age groups, although napping was even more effective in younger compared to older participants. There are no studies, however, directly comparing the effects of caffeine and naps during the day in normally rested individuals, and few that have compared caffeine and sleep at any time for cognitive processes beyond attention, vigilance, or driving. Here, we compared the effects of caffeine, a daytime nap, or placebo on three distinct memory processes: declarative verbal memory, procedural motor skills, and perceptual learning. For verbal memory, we tested recall and recognition in two different phases: 7 h retention with a between-session intervention (caffeine, placebo or nap), and 20 min retention for a different list of words post-intervention. The non-declarative tasks (finger tapping task (FTT) and texture discrimination task (TDT)) were trained before the intervention and then retested afterwards.
Section snippets
Subjects
61 adults between ages 18–39 with no personal history of neurological, psychological or other chronic illness (non-smoking) gave informed consent to participate in the experiment, which was approved by the institutional review boards of the University of California San Diego. Subjects were low to moderate caffeine drinkers (no more that two cups of coffee per day). Since restricted nighttime sleep can have a deleterious effect on performance [31], we required that subjects maintain a sleep
Verbal task
Our main outcome of interest involved the recall and recognition memory scores for the 7 h retention interval, since that interval included the different interventions. To examine that, we utilized a one-way analysis of variance (ANOVA) using three levels of the variable Group (caffeine, nap, placebo), separately for recall and recognition. One concern with this approach, though, would be whether the three groups showed equal performance at baseline (i.e., 20 min memory for Word List 1). Thus, we
Verbal task
No significant differences were found between groups in Recall of Word List 1 at 20 min (Recall means and standard deviations = 13.70(3.0), 15.25(3.33), 12.25(3.5) for placebo, nap, caffeine, respectively; F = 2.36, p = 0.11, eta2 = 0.12) or recognition of Word List 1 at 20 min (recognition means and standard deviations = 4.5(0.99), 4.9(0.60), 4.5(0.73), for placebo, nap, caffeine, respectively; F = 0.73, p = 0.49, eta2 = 0.04). Recall memory for Word List 1 after 7 h retention interval showed significant group
Discussion
In this study, we find that a moderate dose of caffeine impaired motor sequence learning and declarative verbal memory compared to placebo and daytime sleep. These decreases were found despite the fact that caffeine increased subjective alertness, suggesting that the caffeine dose was sufficiently high to have some psychoactive effect. An afternoon nap, on the other hand, improved free recall memory relative to the caffeine group after both a 20 min and a 7 h retention interval and produced
Limitations and caveats
One limitation of this study is that only one dose of caffeine was administered. Thus, the findings should not be generalized beyond this single dose of caffeine, roughly equivalent to two–three cups of coffee. Future studies using multiple doses may show a dose-response effect on motor and verbal memory. It is possible that a group receiving either a higher or lower (than 200 mg) dose of caffeine would exhibit more optimal arousal states and relatively improved performance relative to the
Conclusion
Overall, a daytime nap generally improved performance across three different learning paradigms, while caffeine impaired (or at least did not benefit) performance. We hypothesize that the pattern of results demonstrated by the caffeine group may be explained by the relative level of explicit information in each memory task. The three tasks, perceptual learning, procedural motor skill, and verbal memory, each have varying levels of explicit information involved in learning. The perceptual
Acknowledgments
We would like to acknowledge Kathy Resovsky, Ryan Wong, Arlene Schlosser for help conducting the study; Robert Stickgold and John Wixted for their thoughtful comments. Research was supported by DARPA award # N0014-06-1-0660, the UCSD GCRC M01 RR00827, K01 MH080992-01, R01-AG024506.
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