Preoperative recovery sleep ameliorates postoperative cognitive dysfunction aggravated by sleep fragmentation in aged mice by enhancing EEG delta-wave activity and LFP theta oscillation in hippocampal CA1
Sleep fragmentation (SF) is a common sleep problem experienced during the perioperative period by older adults, and is associated with postoperative cognitive dysfunction (POCD). Increasing evidence indicates that delta-wave activity during non-rapid eye movement (NREM) sleep is involved in sleep-de...
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Published in | Brain research bulletin Vol. 211; p. 110945 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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01.06.2024
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Abstract | Sleep fragmentation (SF) is a common sleep problem experienced during the perioperative period by older adults, and is associated with postoperative cognitive dysfunction (POCD). Increasing evidence indicates that delta-wave activity during non-rapid eye movement (NREM) sleep is involved in sleep-dependent memory consolidation and that hippocampal theta oscillations are related to spatial exploratory memory. Recovery sleep (RS), a self-regulated state of sleep homeostasis, enhances delta-wave power and memory performance in sleep-deprived older mice. However, it remains unclear whether RS therapy has a positive effect on cognitive changes following SF in older mouse models. Therefore, this study aimed to explore whether preoperative RS can alleviate cognitive deficits in aged mice with SF. A model of preoperative 24-h SF combined with exploratory laparotomy-induced POCD was established in 18-month-old mice. Aged mice were treated with preoperative 6-h RS following SF and postoperative 6-h RS following surgery, respectively. The changes in hippocampus-dependent cognitive function were investigated using behavioral tests, electroencephalography (EEG), local field potential (LFP), magnetic resonance imaging, and neuromorphology. Mice that underwent 24-h SF combined with surgery exhibited severe spatial memory impairment; impaired cognitive performance could be alleviated by preoperative RS treatment. In addition, preoperative RS increased NREM sleep; enhanced EEG delta-wave activity and LFP theta oscillation in the hippocampal CA1; and improved hippocampal perfusion, microstructural integrity, and neuronal damage. Taken together, these results provide evidence that preoperative RS may ameliorate the severity of POCD aggravated by SF by enhancing delta slow-wave activity and hippocampal theta oscillation, and by ameliorating the reduction in regional cerebral blood flow and white matter microstructure integrity in the hippocampus.
•Preoperative recovery sleep alleviated postoperative cognitive performance by improving hippocampal perfusion and microstructural connectivity and integrity.•NREM sleep and delta wave power increased during recovery sleep following SF preoperatively.•Preoperative recovery sleep improved hippocampal CA1 theta oscillation in Y-maze task. |
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AbstractList | Sleep fragmentation (SF) is a common sleep problem experienced during the perioperative period by older adults, and is associated with postoperative cognitive dysfunction (POCD). Increasing evidence indicates that delta-wave activity during non-rapid eye movement (NREM) sleep is involved in sleep-dependent memory consolidation and that hippocampal theta oscillations are related to spatial exploratory memory. Recovery sleep (RS), a self-regulated state of sleep homeostasis, enhances delta-wave power and memory performance in sleep-deprived older mice. However, it remains unclear whether RS therapy has a positive effect on cognitive changes following SF in older mouse models. Therefore, this study aimed to explore whether preoperative RS can alleviate cognitive deficits in aged mice with SF. A model of preoperative 24-h SF combined with exploratory laparotomy-induced POCD was established in 18-month-old mice. Aged mice were treated with preoperative 6-h RS following SF and postoperative 6-h RS following surgery, respectively. The changes in hippocampus-dependent cognitive function were investigated using behavioral tests, electroencephalography (EEG), local field potential (LFP), magnetic resonance imaging, and neuromorphology. Mice that underwent 24-h SF combined with surgery exhibited severe spatial memory impairment; impaired cognitive performance could be alleviated by preoperative RS treatment. In addition, preoperative RS increased NREM sleep; enhanced EEG delta-wave activity and LFP theta oscillation in the hippocampal CA1; and improved hippocampal perfusion, microstructural integrity, and neuronal damage. Taken together, these results provide evidence that preoperative RS may ameliorate the severity of POCD aggravated by SF by enhancing delta slow-wave activity and hippocampal theta oscillation, and by ameliorating the reduction in regional cerebral blood flow and white matter microstructure integrity in the hippocampus. Sleep fragmentation (SF) is a common sleep problem experienced during the perioperative period by older adults, and is associated with postoperative cognitive dysfunction (POCD). Increasing evidence indicates that delta-wave activity during non-rapid eye movement (NREM) sleep is involved in sleep-dependent memory consolidation and that hippocampal theta oscillations are related to spatial exploratory memory. Recovery sleep (RS), a self-regulated state of sleep homeostasis, enhances delta-wave power and memory performance in sleep-deprived older mice. However, it remains unclear whether RS therapy has a positive effect on cognitive changes following SF in older mouse models. Therefore, this study aimed to explore whether preoperative RS can alleviate cognitive deficits in aged mice with SF. A model of preoperative 24-h SF combined with exploratory laparotomy-induced POCD was established in 18-month-old mice. Aged mice were treated with preoperative 6-h RS following SF and postoperative 6-h RS following surgery, respectively. The changes in hippocampus-dependent cognitive function were investigated using behavioral tests, electroencephalography (EEG), local field potential (LFP), magnetic resonance imaging, and neuromorphology. Mice that underwent 24-h SF combined with surgery exhibited severe spatial memory impairment; impaired cognitive performance could be alleviated by preoperative RS treatment. In addition, preoperative RS increased NREM sleep; enhanced EEG delta-wave activity and LFP theta oscillation in the hippocampal CA1; and improved hippocampal perfusion, microstructural integrity, and neuronal damage. Taken together, these results provide evidence that preoperative RS may ameliorate the severity of POCD aggravated by SF by enhancing delta slow-wave activity and hippocampal theta oscillation, and by ameliorating the reduction in regional cerebral blood flow and white matter microstructure integrity in the hippocampus. •Preoperative recovery sleep alleviated postoperative cognitive performance by improving hippocampal perfusion and microstructural connectivity and integrity.•NREM sleep and delta wave power increased during recovery sleep following SF preoperatively.•Preoperative recovery sleep improved hippocampal CA1 theta oscillation in Y-maze task. |
ArticleNumber | 110945 |
Author | Zhao, Lina Li, Yun Long, Siwen Li, Yize Hou, Shaowei Li, Feixiang Yu, Yonghao Yang, Yue |
Author_xml | – sequence: 1 givenname: Yun surname: Li fullname: Li, Yun organization: Department of Anesthesiology, Tianjin Medical University General Hospital, Tianjin 300052, China – sequence: 2 givenname: Shaowei surname: Hou fullname: Hou, Shaowei organization: School of Biomedical Engineering and Technology, Tianjin Medical University, Tianjin 300070, China – sequence: 3 givenname: Feixiang surname: Li fullname: Li, Feixiang organization: Department of Anesthesiology, Tianjin Medical University General Hospital, Tianjin 300052, China – sequence: 4 givenname: Siwen surname: Long fullname: Long, Siwen organization: Department of Anesthesiology, Tianjin Medical University General Hospital, Tianjin 300052, China – sequence: 5 givenname: Yue surname: Yang fullname: Yang, Yue organization: Department of Anesthesiology, Tianjin Medical University General Hospital, Tianjin 300052, China – sequence: 6 givenname: Yize surname: Li fullname: Li, Yize organization: Department of Anesthesiology, Tianjin Medical University General Hospital, Tianjin 300052, China – sequence: 7 givenname: Lina surname: Zhao fullname: Zhao, Lina email: 18240198229@163.com organization: Department of Critical Care Medicine, Tianjin Medical University General Hospital, Tianjin 300052, China – sequence: 8 givenname: Yonghao orcidid: 0000-0002-7289-7748 surname: Yu fullname: Yu, Yonghao email: yyu@tmu.edu.cn organization: Department of Anesthesiology, Tianjin Medical University General Hospital, Tianjin 300052, China |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38608544$$D View this record in MEDLINE/PubMed |
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Keywords | Recovery sleep Local field potential Sleep fragmentation POCD Delta wave Theta oscillation Electroencephalography Hippocampus |
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SubjectTerms | Aging - physiology Animals CA1 Region, Hippocampal - physiopathology Cognitive Dysfunction - etiology Cognitive Dysfunction - physiopathology Delta Rhythm - physiology Delta wave Electroencephalography Electroencephalography - methods Hippocampus Local field potential Male Mice Mice, Inbred C57BL POCD Postoperative Cognitive Complications Recovery sleep Sleep - physiology Sleep Deprivation - complications Sleep Deprivation - physiopathology Sleep fragmentation Theta oscillation Theta Rhythm - physiology |
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Title | Preoperative recovery sleep ameliorates postoperative cognitive dysfunction aggravated by sleep fragmentation in aged mice by enhancing EEG delta-wave activity and LFP theta oscillation in hippocampal CA1 |
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