Sleep disruption elevates oxidative stress in parvalbumin-positive cells of the rat cerebral cortex

John H Harkness; Priyanka N Bushana; Ryan P Todd; William C Clegern; Barbara A Sorg; Jonathan P Wisor

doi:10.1093/sleep/zsy201

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Sleep disruption elevates oxidative stress in parvalbumin-positive cells of the rat cerebral cortex

Journal article

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Sleep disruption elevates oxidative stress in parvalbumin-positive cells of the rat cerebral cortex

John H Harkness, Priyanka N Bushana, Ryan P Todd, William C Clegern, Barbara A Sorg and Jonathan P Wisor

Sleep (New York, N.Y.), Vol.42(1)

01/01/2019

DOI: https://doi.org/10.1093/sleep/zsy201

Handle:

https://hdl.handle.net/2376/105872

PMCID: PMC6335871

PMID: 30371896

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https://doi.org/10.1093/sleep/zsy201View

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Abstract

8-Hydroxy-2'-Deoxyguanosine - analysis

Oxidative Stress - physiology

Parvalbumins - metabolism

Rats

Male

Prefrontal Cortex - cytology

Rats, Sprague-Dawley

Plant Lectins

Sleep Deprivation - physiopathology

Animals

Prefrontal Cortex - metabolism

Wakefulness - physiology

Receptors, N-Acetylglucosamine

Anxiety

Neurons - metabolism

Sleep - physiology

We used a novel automated sleep disruption (SD) apparatus to determine the impact of SD on sleep and molecular markers of oxidative stress in parvalbumin (PV) neurons in the rat prefrontal cortex (PFC). Rats were subjected to two 6 hr SD sessions from zeitgeber time (ZT) 0 to ZT6, one by the gentle handling method and the other by an automated agitator running the length of the rat's home cage floor (a novel SD method). The same rats were later subjected to a 12 hr SD session from ZT0 to ZT12. Sleep was disrupted with both methods, although rats slept less during gentle handling than during the automated condition. Immediately after both SD sessions, rats displayed compensatory sleep characterized by elevated slow-wave activity. We measured in the prelimbic prefrontal cortex (prelimbic PFC; 6 and 12 hr SD) and orbital frontal cortex (12 hr SD) the intensity of the oxidative stress marker, 8-oxo-2'-deoxyguanosine (8-oxo-dG) as well as the staining intensity of PV and the PV cell-associated perineuronal net marker, Wisteria floribunda agglutinin (WFA). In the prelimbic PFC, 6 hr SD increased the intensity of 8-oxo-dG, PV, and WFA. After 12 hr SD, the intensity of 8-oxo-dG was elevated in all neurons. PV intensity was elevated only in neurons colabeled with 8-oxo-dG or WFA, and no changes were found in WFA intensity. We conclude that in association with SD-induced sleep drive, PV neurons in the prelimbic PFC exhibit oxidative stress.

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Title: Sleep disruption elevates oxidative stress in parvalbumin-positive cells of the rat cerebral cortex
Creators: John H Harkness - Department of Integrative Physiology and Neuroscience, Translational Addiction Research Center, Washington State University, Vancouver, WA
Priyanka N Bushana - Department of Biomedical Sciences, Elson S. Floyd College of Medicine, Spokane, WA
Ryan P Todd - Department of Integrative Physiology and Neuroscience, Translational Addiction Research Center, Washington State University, Vancouver, WA
William C Clegern - Department of Biomedical Sciences, Elson S. Floyd College of Medicine, Spokane, WA
Barbara A Sorg - Department of Integrative Physiology and Neuroscience, Translational Addiction Research Center, Washington State University, Vancouver, WA
Jonathan P Wisor - Department of Biomedical Sciences, Elson S. Floyd College of Medicine, Spokane, WA
Publication Details: Sleep (New York, N.Y.), Vol.42(1)
Academic Unit: Biomedical Sciences, Department of
Publisher: United States
Grant note: R01 NS078498 / NINDS NIH HHS R01 DA040965 / NIDA NIH HHS R01 DA033404 / NIDA NIH HHS
Identifiers: 99900546999701842
Language: English
Resource Type: Journal article