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Randomized Controlled Trial
. 2008 Jan 29:1191:127-35.
doi: 10.1016/j.brainres.2007.10.106. Epub 2007 Nov 28.

Interindividual sleep spindle differences and their relation to learning-related enhancements

Manuel Schabus  1 , Kerstin Hoedlmoser, Thomas Pecherstorfer, Peter Anderer, Georg Gruber, Silvia Parapatics, Cornelia Sauter, Gerhard Kloesch, Wolfgang Klimesch, Bernd Saletu, Josef Zeitlhofer
Affiliations
Randomized Controlled Trial

Interindividual sleep spindle differences and their relation to learning-related enhancements

Manuel Schabus et al. Brain Res. .

Abstract

We reported earlier that overnight change in explicit memory is positively related to the change in sleep spindle activity (between a control and a learning night). However, it remained unclear whether this effect was restricted to good memory performers and whether a general association of sleep spindles and a "sleep-related learning trait" may not account for this effect. Here we now present a secondary and more detailed analysis of our randomized multicenter study. Subjects were studied over a 4-week study period (including actigraphy and daily sleep diaries), including three overnight stays in the sleep laboratory. In the course of the study, subjects completed test-batteries of memory (Wechsler-Memory-Scale-revised; WMS) and other cognitive abilities (Raven's Advanced-Progressive-Matrices; APM) and were asked to study 160 word pairs in the evening before being tested by cued-recall. Afterwards, subjects went to bed in the laboratory with full polysomnographic montages. Additionally, subjects participated on another occasion in a non-learning control (perceptual priming) task that was counterbalanced either before or after the learning condition. Slow as well as fast spindle activities were analyzed at frontopolar and central topographies. Although it was found that spindle activity is generally (in learning as well as control nights) elevated in highly gifted subjects, spindle analyses revealed that spindle increase (control to learning night) is specifically related to explicit memory improvement overnight, independent of individual learning traits. Together these findings suggest that the spindle increase after learning is related to elaborate encoding before sleep, whereas an individual's general learning ability is well reflected in interindividual (and trait-like) differences of absolute sleep spindle activity.

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Figures

Figure 1
Figure 1
Study design. Illustrated are the subjects' five visits (3 PSG nights) to the sleep laboratory separated by one week each. During the whole study period (4 weeks) subjects (N = 24) had to wear wrist actigraphs to monitor their regular sleep-wake cycles and to complete daily sleep diaries. The order of learning and control tasks prior to sleep were counterbalanced across subjects (double-sided arrow) with the (1-week) “follow-up retrieval” session only following the learning task. PSG, polysomnography.
Figure 2
Figure 2
Sleep spindle activity and its relation to memory improvement and cognitive abilities. Upper graphs depict moderately gifted subjects (APM-) and lower graphs highly gifted (APM+) subjects whereas on the left “Non-Improvers” and on the right “Improvers” are shown. Note that highly gifted individuals (APM+) have more activity in the slow spindle frequency band (11-13Hz; marked area) time-locked to the detected spindle onset (t= 0) irrespective of memory improvement group. Colors represent the (mean) “power” (Gabor estimates; arbitrary units) of EEG frequency bands (between 1-30 Hz) with hot (red) colors indicating stronger activity. For the time-frequency graphs all-night (slow and fast) detected sleep spindles from frontopolar recording site Fp1 of the learning were used as “events” of interest.
Figure 3
Figure 3
Spindle activity increase control to learning night is independent of APM performance. Control to learning night enhancement in spindle activity (central topography) seems only to depend on whether subjects are also memory improvers (right) or non-improvers (left) but not whether they are highly (solid) or moderately gifted (dashed line) as tested with the APM test. Furthermore, the overall higher base levels in spindle activity in high cognitive performers (APM+) irrespective of learning condition are evident. Post hoc statistics are indicated where significant. Note that control to learning night enhancements in memory improvers are independent of APM performance; the provided p-value (dark gray) refers to the general increase with both improvement groups collapsed.
Figure 4
Figure 4
Slow and fast spindle activity during control and learning night for memory “Improvers” and “Non-Improvers” (central topography). Note that (i) the (fast) spindle increase control to learning night is dependent upon whether subjects are also memory improvers (solid line) and (ii) that although, memory non-Improvers seem to start of at higher spindle activity levels none of the between subject comparisons turned out to be significant. Mean spindle activity values (± SEM) are depicted. Post hoc statistics are indicated where significant.
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