Vagotomy attenuates brain cytokines and sleep induced by peripherally administered tumor necrosis factor-α and lipopolysaccharide in mice

Mark R Zielinski; Danielle L Dunbrasky; Ping Taishi; Gianne Souza; James M Krueger

doi:10.5665/sleep.2892

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Vagotomy attenuates brain cytokines and sleep induced by peripherally administered tumor necrosis factor-α and lipopolysaccharide in mice

Journal article

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Vagotomy attenuates brain cytokines and sleep induced by peripherally administered tumor necrosis factor-α and lipopolysaccharide in mice

Mark R Zielinski, Danielle L Dunbrasky, Ping Taishi, Gianne Souza and James M Krueger

Sleep (New York, N.Y.), Vol.36(8), pp.1227-1238

08/01/2013

DOI: https://doi.org/10.5665/sleep.2892

Handle:

https://hdl.handle.net/2376/105082

PMCID: PMC3700720

PMID: 23904683

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Abstract

Brain Chemistry - drug effects

Gene Expression - drug effects

Cytokines - analysis

Mice, Inbred C57BL

Male

Sleep Stages - drug effects

Polysomnography

Sleep - drug effects

Cytokines - physiology

Brain Chemistry - physiology

Dose-Response Relationship, Drug

Tumor Necrosis Factor-alpha - pharmacology

Vagus Nerve - physiology

Animals

Vagotomy - methods

Gene Expression - physiology

Lipopolysaccharides - pharmacology

Tumor Necrosis Factor-alpha - physiology

Sleep Stages - physiology

Mice

Sleep - physiology

Systemic tumor necrosis factor-α (TNF-α) is linked to sleep and sleep altering pathologies in humans. Evidence from animals indicates that systemic and brain TNF-α have a role in regulating sleep. In animals, TNF-α or lipopolysaccharide (LPS) enhance brain pro-inflammatory cytokine expression and sleep after central or peripheral administration. Vagotomy blocks enhanced sleep induced by systemic TNF-α and LPS in rats, suggesting that vagal afferent stimulation by TNF-α enhances pro-inflammatory cytokines in sleep-related brain areas. However, the effects of systemic TNF-α on brain cytokine expression and mouse sleep remain unknown. We investigated the role of vagal afferents on brain cytokines and sleep after systemically applied TNF-α or LPS in mice. Spontaneous sleep was similar in vagotomized and sham-operated controls. Vagotomy attenuated TNF-α- and LPS-enhanced non-rapid eye movement sleep (NREMS); these effects were more evident after lower doses of these substances. Vagotomy did not affect rapid eye movement sleep responses to these substances. NREMS electroencephalogram delta power (0.5-4 Hz range) was suppressed after peripheral TNF-α or LPS injections, although vagotomy did not affect these responses. Compared to sham-operated controls, vagotomy did not affect liver cytokines. However, vagotomy attenuated interleukin-1 beta (IL-1β) and TNF-α mRNA brain levels after TNF-α, but not after LPS, compared to the sham-operated controls. We conclude that vagal afferents mediate peripheral TNF-α-induced brain TNF-α and IL-1β mRNA expressions to affect sleep. We also conclude that vagal afferents alter sleep induced by peripheral pro-inflammatory stimuli in mice similar to those occurring in other species.

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Title: Vagotomy attenuates brain cytokines and sleep induced by peripherally administered tumor necrosis factor-α and lipopolysaccharide in mice
Creators: Mark R Zielinski - Sleep and Performance Research Center, Washington State University, Spokane, WA 99210-1495, USA
Danielle L Dunbrasky
Ping Taishi
Gianne Souza
James M Krueger
Publication Details: Sleep (New York, N.Y.), Vol.36(8), pp.1227-1238
Academic Unit: Integrative Physiology and Neuroscience, Department of
Publisher: United States
Grant note: R01 NS025378 / NINDS NIH HHS NS025378 / NINDS NIH HHS R01 NS031453 / NINDS NIH HHS HD036520 / NICHD NIH HHS NS031453 / NINDS NIH HHS R01 HD036520 / NICHD NIH HHS
Identifiers: 99900547082201842
Language: English
Resource Type: Journal article