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The Journal of Neuroscience, August 30, 2006, 26(35):8976-8982; doi:10.1523/JNEUROSCI.2464-06.2006

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Behavioral/Systems/Cognitive
Encoding Difficulty Promotes Postlearning Changes in Sleep Spindle Activity during Napping

Christina Schmidt,^1,2,3 Philippe Peigneux,² Vincenzo Muto,⁴ Maja Schenkel,¹ Vera Knoblauch,¹ Mirjam Münch,¹ Dominique J.-F. de Quervain,⁵ Anna Wirz-Justice,¹ and Christian Cajochen¹

¹Centre for Chronobiology, Psychiatric University Clinics, CH-4025 Basel, Switzerland, ²Cyclotron Research Centre and ³Department of Cognitive Psychology, University of Liège, B-4000 Liège, Belgium, ⁴Department of Psychology, II University of Naples, 81100 Caserta, Italy, and ⁵Division of Psychiatry Research, University of Zurich, CH-8057 Zurich, Switzerland

Correspondence should be addressed to Christian Cajochen, Center for Chronobiology, Psychiatric University Clinics, Wilhelm-Klein Strasse 27, CH-4025 Basel, Switzerland. Email: christian.cajochen{at}upkbs.ch

Learning-dependent increases in sleep spindle density have been reported during nocturnal sleep immediately after the learning session. Here, we investigated experience-dependent changes in daytime sleep EEG activity after declarative learning of unrelated word pairs. At weekly intervals, 13 young male volunteers spent three 24 h sessions in the laboratory under carefully controlled homeostatic and circadian conditions. At approximately midday, subjects performed either one of two word-pair learning tasks or a matched nonlearning control task, in a counterbalanced order. The two learning lists differed in the level of concreteness of the words used, resulting in an easier and a more difficult associative encoding condition, as confirmed by performance at immediate cued recall. Subjects were then allowed to sleep for 4 h; afterward, delayed cued recall was tested. Compared with the control condition, sleep EEG spectral activity in the low spindle frequency range and the density of low-frequency sleep spindles (11.25–13.75 Hz) were both significantly increased in the left frontal cortex after the difficult but not after the easy encoding condition. Furthermore, we found positive correlations between these EEG changes during sleep and changes in memory performance between pre-nap and post-nap recall sessions. These results indicate that, like during nocturnal sleep, daytime sleep EEG oscillations including spindle activity are modified after declarative learning of word pairs. Furthermore, we demonstrate here that the nature of the learning material is a determinant factor for sleep-related alterations after declarative learning.

Key words: daytime sleep; sleep spindles; declarative memory; encoding difficulty; EEG; human

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Received March 31, 2006; revised July 18, 2006; accepted July 18, 2006.

Correspondence should be addressed to Christian Cajochen, Center for Chronobiology, Psychiatric University Clinics, Wilhelm-Klein Strasse 27, CH-4025 Basel, Switzerland. Email: christian.cajochen{at}upkbs.ch

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