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Involvement of sleep spindles in overnight declarative memory stabilization

Effects of time of incidence and spindle type

Die Beteiligung von Schlafspindeln an der nächtlichen Stabilisierung deklarativer Gedächtnisinhalte

Effekte von Spindeltyp und Zeit des Auftretens

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Abstract

Objective

Numerous studies point to the involvement of sleep spindles and slow waves in memory processes, particularly in hippocampus-dependent declarative memory. We have shown previously that the overnight change in recall performance in a declarative word pair association task correlates significantly with increased spindle activity during the night after learning compared to a control night. The current study re-evaluates this relationship in detail and explores whether the observed positive correlation of two spindle parameters measured during stage 2 (S2) sleep with overnight stabilization depend on the time of night (early vs. late) and spindle type (fast vs. slow).

Methods

The study included 24 healthy volunteers aged 20–30 years. Two counterbalanced nights served as either control condition without intentional learning or as an experimental condition including a declarative memory task in the evening. Performance was tested directly after learning and in the following morning. Spindle detection was based on a validated automatic algorithm, providing density and intensity of slow (≤ 13 Hz) and fast (> 13 Hz) spindles per minute S2 sleep. To obtain spindle measures during the course of the night, the entire recording period was segmented into five 90-min parts.

Results

Significant correlations were observed between changes (experimental night minus control night) in spindle density (r = 0.44, p < 0.05) and intensity (r = 0.52, p < 0.01), and overnight changes in memory performance during the night following the learning task. Changes in memory performance correlate significantly with changes in fast spindle intensity (parts 1–3) and density (part 2), but not significantly with any slow spindle parameter.

Conclusion

The present study confirms the involvement of fast sleep spindles during S2 in declarative memory processes. Significant correlations with spindle retention are only seen in early S2 sleep and not during late S2 sleep. It remains to be investigated whether this effect is due to circadian factors, homeostatic factors, or the time elapsed after initial learning.

Zusammenfassung

Fragestellung

Zahlreiche Studien deuten auf eine Beteiligung von Schlafspindeln und langsamen Wellen an Gedächtnisprozessen hin, insbesondere im Bereich des vom Hippocampus abhängigen deklarativen Gedächtnisses. In einer früheren Studie konnten wir zeigen, dass über die Nacht auftretende Veränderungen der Abrufleistung in einer Wortpaar-Assoziationsaufgabe signifikant mit Änderungen der Spindelaktivität zwischen der Lernnacht und einer Kontrollnacht korrelieren. Das Ziel der aktuellen Studie war, diesen Zusammenhang im Detail zu reevaluieren und zu untersuchen, ob die beobachteten positive Korrelationen zweier in Stadium 2 erhobener Spindelparameter mit der nächtlichen Gedächtnisstabilisierung von Zeit der Nacht (früh versus spät) und vom Spindeltyp (schnell versus langsam) abhängig sind.

Methode

24 gesunde Probanden im Alter zwischen 20 und 30 Jahren nahmen an der Untersuchung teil. Zwei in ihrer Reihenfolge randomisierte Nächte dienten entweder als Kontrollbedingung ohne intentionales Lernen oder als Experimentalbedingung mit einer deklarativen Gedächtnisaufgabe am Abend. Die Abrufleistung wurde direkt nach dem Lernen und am darauffolgenden Morgen getestet. Die Spindelerkennung basiert auf einer validierten automatischen Methode und liefert Werte für Spindeldichte und Spindelintensität langsamer (≤ 13 Hz) und schneller (> 13 Hz) Schlafspindeln pro Minute S2-Schlaf. Die gesamte Aufnahme wurde in 5 Teile zu je 90 Minuten segmentiert, um Spindelparameter im Verlauf der Nacht zu beschreiben.

Ergebnisse

Wir beobachteten signifikante Korrelationen zwischen Veränderungen (Experimentalnacht minus Kontrollnacht) hinsichtlich Spindeldichte (r = 0,44, p < 0,05) und Spindelintensität (r = 0,52, p < 0,01) und den Veränderungen der Gedächtnisleistung von abends zu morgens in der Lernnacht. Letztere korrelieren signifikant mit Änderungen der Intensität (Sequenzen 1–3) und Dichte (Sequenz 2) schneller Schlafspindeln jedoch mit keinem der Parameter langsamer Spindeln.

Schlussfolgerung

Zusammenfassend lässt sich sagen, dass die aktuelle Studie für eine Beteiligung schneller in S2 auftretender Schlafspindeln an deklarativen Gedächtnisprozessen spricht. Signifikante Spindel-Abruf Korrelationen finden sich nur im frühen S2-Schlaf, jedoch nicht während des späten S2-Schlafs. Es bleibt noch zu klären, ob dieser Effekt auf zirkadiane Faktoren, homöostatische Faktoren oder auf die seit dem Lernen vergangene Zeit zurückzuführen ist.

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Compliance with ethical guidelines

Conflict of interest. P. Anderer, B. Saletu, and J. Zeitlhofer are shareholders of The Siesta Group Schlafanalyse GmbH; G. Gruber and S. Parapatics are employees of The Siesta Group Schlafanalyse GmbH. M. Schabus, W. Klimesch, G. Klösch, C. Sauter, and B. Saletu state that there are no conflicts of interest. All studies on humans described in the present manuscript were carried out with the approval of the responsible ethics committee and in accordance with national law and the Helsinki Declaration of 1975 (in its current, revised form). Informed consent was obtained from all patients included in studies.

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Gruber, G., Anderer, P., Parapatics, S. et al. Involvement of sleep spindles in overnight declarative memory stabilization. Somnologie 19, 30–37 (2015). https://doi.org/10.1007/s11818-015-0699-8

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