Enhancement of declarative memory performance following a daytime nap is contingent on strength of initial task acquisition.

IT IS BECOMING INCREASINGLY CLEAR THAT NREM SLEEP, ESPECIALLY SLOW WAVE SLEEP (SWS), IS IMPORTANT FOR THE PROCESSING OF HIPPOCAMPUS-dependent declarative memories,1–6 with SWS hypothesized to provide the optimal electrophysiological and biochemical state for this type of processing.7,8 When sleep occurs in the form of a short daytime nap, it is very common to obtain only NREM sleep, without entering REM sleep, which would usually occur at least 90 minutes into the sleep period. The few studies examining the effect of daytime naps on memory have made use of this knowledge, demonstrating that daytime naps containing only NREM sleep (including SWS) facilitate verbal declarative memory (semantically related paired associates),9 with one study showing that paired associates improvement is contingent on whether subjects obtained SWS during the nap.10 These findings represent a first step forward in our understanding of how daytime naps benefit declarative memory processing. However, there are many questions still to be explored. To this end, the present study examines the benefits of a daytime NREM nap on a spectrum of declarative memory tasks, and begins to assess the importance of factors related to task acquisition and their potential to modulate sleep-related memory processing. To more broadly assess the declarative memory benefits of NREM sleep obtained during a daytime nap, subjects were trained on 3 well-known declarative (hippocampus-dependent) memory tasks. The first task was an unrelated paired associates task, a more difficult counterpart to the commonly used related paired associates task.3,4 The task comprises pairs of common words that lack an inherent semantic relationship (e.g., shirt–paper). Two nonverbal declarative memory tasks that do not rely strongly on previously learned concepts were also evaluated: the Rey-Osterrieth complex figure test (ROCFT; a measure of visuospatial declarative memory) and a maze learning task adapted from the task used by Brenda Milner on a large sample of hippocampal lesion patients including HM.11 Both of these tasks are void of semantically charged landmarks, objects, or verbal material that would have been previously learned by subjects. To date, no studies have used this particular maze learning task, and only 2 have examined the effect of sleep on memory using the ROCFT. In epileptic patients it was shown that performance on the ROCFT correlated positively with low frequency EEG spectral power (<1.25 Hz) overnight,12 and in schizophrenic patients the amount of SWS correlated positively with overnight ROCFT performance.13 In the present study we also explored the extent to which different methods of information encoding modulate the effect of sleep on memory. The impetus for exploring encoding factors was based on two studies by Smith, et al.14,15 who found that only when rats successfully acquired an operant conditioning or passive avoidance task was there an increase in subsequent paradoxical sleep. These findings suggested for the first time that the extent of task acquisition may be an important modulator of the effect of sleep on memory processing. Support for this general finding comes from a recent PET study demonstrating that the strength of acquisition of a serial reaction time task is correlated with increased brain activation (regional cerebral blood flow) during post-acquisition REM sleep.16 Similarly, it was shown that stronger acquisition of a motor adaptation task not only correlates with an increase in slow wave activity (SWA) during subsequent sleep, but this increase in SWA is correlated with enhanced performance following sleep.17 Given these findings, it becomes clear that the individual's success in acquiring a task may be an important factor in understanding how sleep facilitates memory formation. In addition to the assessment of individual differences in acquisition, the level of task acquisition can be experimentally manipulated to assess the preferential effect of sleep for information that is more strongly acquired. A recent study by Schmidt et al.18 has shown that not only does spindle density increase significantly during a daytime nap following the encoding of a difficult (but not an easy) paired associates task, but that this increase in spindle density correlates with improvement in paired associates recall. To assess the importance of task acquisition in modulating sleep-related memory processing, we created 2 encoding conditions within the paired associates task. To date, almost all sleep-dependent consolidation studies have employed a “study-test” paradigm,19 whereby subjects learn a list of word pairs, and then perform cued recall tests until a specified performance criterion is met (e.g., 60% correct or one perfect recall trial2,3,20). However, it is still unclear whether immediate testing leads to enhanced paired associates encoding, which in turn allows sleep to more strongly facilitate memory processing, or whether sleep imparts the same performance benefits to subjects that simply learn the word pairs without immediate testing. Interestingly, in a recent study that did not examine sleep/wake differences it was shown that when subjects were tested immediately after learning declarative information (a text passage), recall after one week was superior to recall of subjects that underwent multiple study sessions without being tested.19 To add to our understanding of the nature of task acquisition and its potential to modulate the effects of sleep on memory, subjects in the present study were immediately tested on a subset of the word pairs during the training session (referred to as “tested” word pairs), while the remaining word pairs were studied without immediate test (referred to as “untested” word pairs). In the present study, performance on all 3 declarative tasks was assessed following a 3.5-h training-retest interval that included a daytime NREM nap or no nap. To test the extent to which task acquisition factors modulate sleep-related memory processing, subjects were not only exposed to 2 modes of paired associates encoding, but for each task subjects were also divided post hoc into high and low performers based on training performance (i.e., those performing in the top and bottom half of the sample based on a median split). This allowed for an analysis of the effect of the subjects' ability to acquire each of the 3 tasks as well as the effect of 2 different modes of paired associates acquisition (tested vs. untested) on sleep-related memory processing.