The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical Injury
Traumatic brain injury (TBI) is a significant risk factor for the development of sleep and circadian rhythm impairments. In this study we compare the circadian rhythms and sleep patterns in the high-frequency head impact (HFHI) and controlled cortical impact (CCI) mouse models of TBI. These mouse mo...
Main Authors: | , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2022-07-01
|
Series: | Biology |
Subjects: | |
Online Access: | https://www.mdpi.com/2079-7737/11/7/1031 |
_version_ | 1827597881528287232 |
---|---|
author | Holly T. Korthas Bevan S. Main Alex C. Harvey Ruchelle G. Buenaventura Evan Wicker Patrick A. Forcelli Mark P. Burns |
author_facet | Holly T. Korthas Bevan S. Main Alex C. Harvey Ruchelle G. Buenaventura Evan Wicker Patrick A. Forcelli Mark P. Burns |
author_sort | Holly T. Korthas |
collection | DOAJ |
description | Traumatic brain injury (TBI) is a significant risk factor for the development of sleep and circadian rhythm impairments. In this study we compare the circadian rhythms and sleep patterns in the high-frequency head impact (HFHI) and controlled cortical impact (CCI) mouse models of TBI. These mouse models have different injury mechanisms key differences of pathology in brain regions controlling circadian rhythms and EEG wave generation. We found that both HFHI and CCI caused dysregulation in the diurnal expression of core circadian genes (<i>Bmal1</i>, <i>Clock</i>, <i>Per1</i>,<i>2</i>, <i>Cry1</i>,<i>2</i>) at 24 h post-TBI. CCI mice had reduced locomotor activity on running wheels in the first 7 d post-TBI; however, both CCI and HFHI mice were able to maintain circadian behavior cycles even in the absence of light cues. We used implantable EEG to measure sleep cycles and brain activity and found that there were no differences in the time spent awake, in NREM or REM sleep in either TBI model. However, in the sleep states, CCI mice have reduced delta power in NREM sleep and reduced theta power in REM sleep at 7 d post-TBI. Our data reveal that different types of brain trauma can result in distinct patterns of circadian and sleep disruptions and can be used to better understand the etiology of sleep disorders after TBI. |
first_indexed | 2024-03-09T03:41:39Z |
format | Article |
id | doaj.art-987c63714e934e91b974e82c26918d11 |
institution | Directory Open Access Journal |
issn | 2079-7737 |
language | English |
last_indexed | 2024-03-09T03:41:39Z |
publishDate | 2022-07-01 |
publisher | MDPI AG |
record_format | Article |
series | Biology |
spelling | doaj.art-987c63714e934e91b974e82c26918d112023-12-03T14:40:37ZengMDPI AGBiology2079-77372022-07-01117103110.3390/biology11071031The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical InjuryHolly T. Korthas0Bevan S. Main1Alex C. Harvey2Ruchelle G. Buenaventura3Evan Wicker4Patrick A. Forcelli5Mark P. Burns6Interdisciplinary Program in Neuroscience, Georgetown University Medical Center, Washington, DC 20057, USADepartment of Neuroscience, Georgetown University Medical Center, Washington, DC 20057, USADepartment of Neuroscience, Georgetown University Medical Center, Washington, DC 20057, USADepartment of Neuroscience, Georgetown University Medical Center, Washington, DC 20057, USADepartment of Pharmacology and Physiology, Georgetown University Medical Center, Washington, DC 20057, USAInterdisciplinary Program in Neuroscience, Georgetown University Medical Center, Washington, DC 20057, USAInterdisciplinary Program in Neuroscience, Georgetown University Medical Center, Washington, DC 20057, USATraumatic brain injury (TBI) is a significant risk factor for the development of sleep and circadian rhythm impairments. In this study we compare the circadian rhythms and sleep patterns in the high-frequency head impact (HFHI) and controlled cortical impact (CCI) mouse models of TBI. These mouse models have different injury mechanisms key differences of pathology in brain regions controlling circadian rhythms and EEG wave generation. We found that both HFHI and CCI caused dysregulation in the diurnal expression of core circadian genes (<i>Bmal1</i>, <i>Clock</i>, <i>Per1</i>,<i>2</i>, <i>Cry1</i>,<i>2</i>) at 24 h post-TBI. CCI mice had reduced locomotor activity on running wheels in the first 7 d post-TBI; however, both CCI and HFHI mice were able to maintain circadian behavior cycles even in the absence of light cues. We used implantable EEG to measure sleep cycles and brain activity and found that there were no differences in the time spent awake, in NREM or REM sleep in either TBI model. However, in the sleep states, CCI mice have reduced delta power in NREM sleep and reduced theta power in REM sleep at 7 d post-TBI. Our data reveal that different types of brain trauma can result in distinct patterns of circadian and sleep disruptions and can be used to better understand the etiology of sleep disorders after TBI.https://www.mdpi.com/2079-7737/11/7/1031sleepcircadian rhythmtraumatic brain injury (TBI)mild TBI (mTBI)concussion |
spellingShingle | Holly T. Korthas Bevan S. Main Alex C. Harvey Ruchelle G. Buenaventura Evan Wicker Patrick A. Forcelli Mark P. Burns The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical Injury Biology sleep circadian rhythm traumatic brain injury (TBI) mild TBI (mTBI) concussion |
title | The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical Injury |
title_full | The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical Injury |
title_fullStr | The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical Injury |
title_full_unstemmed | The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical Injury |
title_short | The Effect of Traumatic Brain Injury on Sleep Architecture and Circadian Rhythms in Mice—A Comparison of High-Frequency Head Impact and Controlled Cortical Injury |
title_sort | effect of traumatic brain injury on sleep architecture and circadian rhythms in mice a comparison of high frequency head impact and controlled cortical injury |
topic | sleep circadian rhythm traumatic brain injury (TBI) mild TBI (mTBI) concussion |
url | https://www.mdpi.com/2079-7737/11/7/1031 |
work_keys_str_mv | AT hollytkorthas theeffectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT bevansmain theeffectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT alexcharvey theeffectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT ruchellegbuenaventura theeffectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT evanwicker theeffectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT patrickaforcelli theeffectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT markpburns theeffectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT hollytkorthas effectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT bevansmain effectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT alexcharvey effectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT ruchellegbuenaventura effectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT evanwicker effectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT patrickaforcelli effectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury AT markpburns effectoftraumaticbraininjuryonsleeparchitectureandcircadianrhythmsinmiceacomparisonofhighfrequencyheadimpactandcontrolledcorticalinjury |