Effects of Early and Late Nocturnal Sleep on Declarative and Procedural Memory Werner Plihal and Jan Born University of Bamberg, FRG Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/9/4/534/1754819/jocn.1997.9.4.534.pdf by guest on 18 May 2021 Abstract 1 Recall of paired-associate lists (declarative memory) and early sleep, and recall of mirror-tracing skills improved more mirror-tracing skills (procedural memory) was assessed after during late sleep. The effects may reflect different influences retention intervals defined over early and late nocturnal sleep. of slow wave sleep (SWS) and rapid eye movement @EM) In addition, effects of sleep on recall were compared with sleep since time in SWS was 5 times longer during the early those of early and late retention intervals filled with wakeful- than late sleep retention interval, and time in REM sleep was ness. Twenty healthy men served as subjects. Saliva cortisol twice as long during late than early sleep @ < 0.005).Changes concentrations were determined before and after the retention in cortisol concentrations, which independently of sleep and intervals to determine pituitary-adrenal secretory activity.Sleep wakefulness were lower during early retention intervals than was determined somnopolygraphically. Sleep generally en- late ones, cannot account for the effects of sleep on memory. hanced recall when compared with the effects of correspond- The experiments for the first time dissociate specific effects of ing retention intervals of wakefulness. The benefit from sleep early and late sleep on two principal types of memory, decla- on recall depended on the phase of sleep and on the type of rative and procedural, in humans. H memory: Recall of paired-associate lists improved more during INTRODUCTION practice sessions subjects learned to make the discrimi- nation with shorter exposure times of the stimulus Numerous studies in animals and humans have sug- configuration. While subjects still improved on this task gested that an essential function of sleep is the strength- following a night of SWS deprivation, deprivation of REM ening of memories (e.g., Cipolli, 1995; Dujardien, sleep completely abolished any beneficial effect of sleep. Guerrien, & Leconte, 1990). The sleep-dependent mecha- These results led the authors to suggest that REM sleep nisms underlying memory facilitation, however, are still facilitates the consolidation of procedural memory (i.e., poorly understood. Most studies approaching this issue memories considered to stem from repeated practicing have focused on the role of different sleep stages for of tasks of perceptual or motor skill learning; Squire, memory consolidation, and findings from these studies 1992). have merged into a still ongoing discussion contrasting Despite the large body of positive findings, quite a few the functions of slow wave sleep (SWS) and rapid eye studies failed to demonstrate impairing effects of REM movement @EM) sleep in memory formation and con- sleep deprivation on human memory mainly in tasks of solidation (Dujardien et al., 1990). declarative memory (e.g., Ekstrand, Sullivan, Parker, Sr Mnemonic effects related to REM sleep have been West, 1971; Levin & Glaubman, 1975). In light of these mainly investigated in studies employing REM sleep dep- inconsistencies,it has been questioned whether the dep- rivation (for review, see Levin & Glaubman, 1975). In rivation of REM sleep is the most appropriate way to humans, impairment of memory following REM sleep identify the role of this sleep stage for memory pro- deprivation has been observed in a great variety of tasks cesses. The disruption of REM sleep may per se affect involving declarative memory, such as the recall of sen- cognitive and emotive aspects of stimulus processing tences and stories (e.g., Empson & Clarke, 1970;Tilley & more than disruption of any other sleep stage and may Empson, 1978). However, a strong deleterious effect of thus obscure the functions of this sleep stage essential REM sleep deprivation on memory has been recently for retention processes (Cipolli, 1995). This objection reported also for recall of procedural memories (Karni, appears to be supported by the fact that studies that did Tanne, Rubenstein, Askenasy, & Sagi, 1994). Those authors not employ selective sleep deprivation techniques over- trained subjects to discriminate the orientation of a all suggested a more positive effect on retention of SWS configuration of visually presented lines. With repeated than of REM sleep (Barrett & Ekstrand, 1972; Ekstrand, 0 I997 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 94,pp. 534-547 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.1997.9.4.534 by guest on 30 September 2021 Barrett, West, & Maier, 1977;Fowler, Sullivan, & Ekstrand, RESULTS 1973;Yaroush, Sullivan, & Ekstrand, 1971). In those stud- Sleep ies, retention rates following undisturbed early and late nocturnal sleep were compared. If learning was followed Results from sleep recordings are summarized in Table by a 4-h retention interval placed in the early period of 1. Sleep time between the learning and recall period was nocturnal sleep characterized by extended epochs of nearly identical during the “early sleep” (189.65 f 7.68 SWS, recall of word pairs was superior to recall after a min) and “late sleep’’ condition (188.55 f 6.45 min). 4-h retention interval placed in the REM sleep predomi- However, sleep architecture substantially differed be- nated late period of sleep. However, evidence for an ad- tween both conditions. Time spent in SWS was about 5 vantage of SWS over REM sleep on memory consolidation times longer during early sleep than during late sleep Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/9/4/534/1754819/jocn.1997.9.4.534.pdf by guest on 18 May 2021 provided by examinations of periods of undisturbed (refer to Table 1 for statistical results). In contrast,during early and late nocturnal sleep so far is based solely on early sleep, time spent in REM sleep on the average an assessment of declarative memories. Tasks of proce- reached only 35% of the time spent in this sleep stage dural memory have not been employed with this strategy. during late sleep. Sleep onset latency and latencies of the However, it is important to point out in this context different sleep stages were not different for the early and that early and late nocturnal sleep apart from the diver- late sleep conditions. gent distribution of SWS and REM sleep differ also with Both the condition of late sleep and late wake were respect to other factors that might well influence mem- preceded by 3-h intervals of sleep. Sleep in these inter- ory consolidation. Thus, secretory activity within the vals (prior to the learning period) were comparable, hypothalamo-pituitary-adrenal (HPA) system is at a mini- except that time in stage 1 sleep was slightly enhanced mum during the early part of nocturnal sleep and in the late wake condition. However, this difference did reaches a diurnal maximum in the late part of the night. not reach the 5% level of significance. This secretory pattern very likely reflects a tonic regula- tory influence of the septo-hippocampal system on the Cortisol HPA axis (Born, Steinbach,Dodt, & Fehm, 1997;De Kloet, 1991 ; De Kloet & Reul, 1987). Interestingly, several stud- Cortisol concentrations were substantially lower during ies in awake healthy humans indicated that high plasma the early sleep retention interval (0.34 f 0.13 pg/dl) than corticosteroid concentrations impair declarative mem- during late sleep retention interval (0.64 f 0.09 pg/dl; ory (eg,Kirschbaum, Wolf, May, Wippich,& Hellhammer, F(1, 9) = 7.29,p c 0.05). A parallel difference was ob- 1996; Newcomer, Craft, Hershey, Askins, & Bardgett, served in the wake control group with markedly lower 1994).This influence is probably mediated via binding to cortisol concentrations during the early wake (0.34 f hippocampal corticosteroid receptors (e.g., Bliss & 0.09 pg/dl) than during the late wake retention interval Collingridge, 1993; Oitzel & De Kloet, 1992), and it may (0.91 k 0.17; F(1, 9) = 13.47, p < 0.01). Differences express itself also in a differential impairment of recall between the experimental sleep group and the wake following early and late nocturnal sleep. control group for the corresponding early and late reten- The present study was designed to compare the role tion intervals were not significant (F(1, 18) = 0.00 and of early nocturnal sleep, dominated by SWS, and of late F(1, 18) = 1.82 for the early and the late night, respec- sleep, dominated by REM sleep, for the consolidation of tively). declarative and procedural memory. Since the selective dependency of procedural memory from REM sleep, so Paired-Associate far, has been shown only in the context of REM sleep Lists deprivation procedures, it was of particular interest to Table 2 summarizes results from performance on paired- examine whether procedural memory would improve associate lists for the learning and recall period of the also from undisturbed late sleep to a greater extent than four retention conditions (early sleep, late sleep, early from undisturbed early sleep. For this purpose, healthy wake, late wake). In the experimental sleep group, com- men were first trained (to a criterion) in recall of a parison of performance during the learning period (as paired-associate word list (a task of declarative memory) indicated by the number of trails until the criterion of and in a mirror-tracing task (a procedural memory task). 60% correct responses was reached and by the number Recall was again tested after 3-h retention intervals po- of correct responses during the final learning trial) did sitioned during early and during late sleep and also after not indicate any systematic difference between the con- corresponding intervals of wakefulness. In addition, ditions of early and late sleep.