Postoperative 24-h Acute Sleep Deprivation Improves Learning and Memory Through Inhibition of Tau Phosphorylation in the Hippocampal Neurons of Splenectomized Rats

Abstract

Purpose

As tau pathology is involved in impaired postoperative learning and memory in rats, we attempted to identify the possible mechanisms by which tau pathology affects postoperative sleep deprivation.

Methods

Adult male Sprague-Dawley rats were randomly assigned into six groups as follows: the Control group, Anaesthesia group, Surgery group, Sleep deprivation (SD) group: 24-h SD with the modified multiple platform method (MMPM), Anaesthesia and SD (ASD) group, and Surgery and SD (SSD) group. Tau396 and FOXQ1 protein expression levels in the hippocampal neurons of all groups were analysed. Changes following co-culture of hippocampal neurons with IL-6 were detected by flow cytometry.

Results

Twenty-four hours of acute SD decreased the error scores on postoperative day 5 in the ASD and SSD groups compared with the Anaesthesia and Surgery groups. Compared with the tau levels in the Control group, tau levels in the Anaesthesia and Surgery groups were increased, but SD decreased the expression of tau in the ASD and SSD groups. The expression levels of tau and FOXQ1 were inversely regulated. When hippocampal neurons were co-cultured with IL-6, the same changes were observed.

Conclusion

Postoperative 24-h acute SD improves learning and memory through inhibition of tau phosphorylation and increases IL-6-induced expression of FOXQ1 in the hippocampal neurons of splenectomized rats.

Keywords:

• tau pathology
• interleukin-6
• postoperative sleep deprivation
• FOXQ1
• learning
• memory

Abbreviations

SD, sleep deprivation; ASD, anaesthesia and sleep deprivation; SSD, surgery and sleep deprivation; MMPM, modified multiple platform method; IL-6, interleukin-6; FOX, Forkhead box; BBB, blood–brain barrier; EB, Evans blue; ANOVA, one-way analysis of variance.

Data Sharing Statement

Datasets are available on request.

Author Contributions

All authors substantially contributed to the conception and design of the study, data acquisition, or analysis and interpretation of the data, participated in drafting the article or revising it critically for important intellectual content, provided final approval of the version to be published, and agree to be accountable for all aspects of the work.

Disclosure

The authors declare that they have no competing interests for this work.

Additional information

Funding

This work was funded by the Natural Science Foundation of Liaoning Province (20180551176) to Wen-fei Tan, the Fund for Scientific Research of the First Hospital of China Medical University (FHCMU- FSR) to Wen-fei Tan and the National Natural Science Foundation of China (No. 81601053) to Xiao-qian Li.