The influence of rapid eye movement sleep deprivation on nociceptive transmission and the duration of facial allodynia in rats: a behavioral and Fos immunohistochemical study

There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

Abstract

Background

Disrupted sleep is associated with a reciprocal influence on headaches and is one of the contributing factors in the process of chronicity. The goal of the present study was to investigate the influence of sleep on headaches using animal rapid eye movement (REM) sleep deprivation and supradural capsaicin infusion models.

Method

Sprague-Dawley rats underwent REM sleep deprivation (REMSD) for 96 h. The sensory threshold to mechanical stimuli, assessed by the von Frey monofilament test, was measured during the REMSD period. Additionally, the Fos protein expression level was measured in the trigeminocervical complex, periaqueductal gray, and hypothalamus. Following supradural infusion of capsaicin, we evaluated the duration of facial allodynia for 28 days after REMSD.

Results

After REMSD, the sensory threshold to mechanical stimuli was significantly decreased ( p < 0.01) and Fos-positivity in the posterior ( p = 0.010) and dorsomedial hypothalamus ( p = 0.024), ventrolateral periaqueductal gray ( p = 0.016), and superficial layer of the trigeminocervical complex ( p = 0.019) were significantly increased. The duration of facial allodynia induced by supradural capsaicin infusion was significantly longer in the REM sleep deprivation and capsaicin infusion group (Day 10 PSD vs. Day 25 PSD).

Conclusion

The present study demonstrates that REM sleep deprivation increased nociceptive transmission from trigeminal nerve endings. Furthermore, it suggests that sleep deprivation may contribute to the chronicity of facial allodynia.

Related collections

Most cited references 43

Record: found
Abstract: found
Article: not found

Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning.

Laurel A Graves, Elizabeth A Heller, Allan I. Pack … (2003)

Many behavioral and electrophysiological studies in animals and humans have suggested that sleep and circadian rhythms influence memory consolidation. In rodents, hippocampus-dependent memory may be particularly sensitive to sleep deprivation after training, as spatial memory in the Morris water maze is impaired by rapid eye movement sleep deprivation following training. Spatial learning in the Morris water maze, however, requires multiple training trials and performance, as measured by time to reach the hidden platform is influenced by not only spatial learning but also procedural learning. To determine if sleep is important for the consolidation of a single-trial, hippocampus-dependent task, we sleep deprived animals for 0-5 and 5-10 h after training for contextual and cued fear conditioning. We found that sleep deprivation from 0-5 h after training for this task impaired memory consolidation for contextual fear conditioning whereas sleep deprivation from 5-10 h after training had no effect. Sleep deprivation at either time point had no effect on cued fear conditioning, a hippocampus-independent task. Previous studies have determined that memory consolidation for fear conditioning is impaired when protein kinase A and protein synthesis inhibitors are administered at the same time as when sleep deprivation is effective, suggesting that sleep deprivation may act by modifying these molecular mechanisms of memory storage.

0 comments Cited 121 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: not found

Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve.

BP Vos, AM Strassman, RJ Maciewicz (1994)

Video recordings of free behavior and responses to mechanical facial stimulation were analyzed to assess whether chronic constriction injury (CCI) to the rat's infraorbital nerve (IoN) results in behavioral alterations indicative of neuropathic pain. A unilateral CCI was produced by placing loose chromic gut ligatures around the IoN. After CCI to the IoN, rats exhibited changes in both non-evoked and evoked behavior. Behavioral changes developed in two phases. Early after CCI (postoperative days 1-15), rats showed increased face-grooming activity with face-wash strokes directed to the injured nerve territory, while the responsiveness to stimulation of this area was decreased. Later after CCI (postoperative days 15-130), the prevalence of asymmetric face grooming was reduced but remained significantly increased compared to control rats. The early hyporesponsiveness was abruptly replaced by an extreme hyperresponsiveness: all stimulus intensities applied to the injured nerve territory evoked the "maximal" response (brisk head withdrawal, avoidance behavior plus directed face grooming). This response was never observed in control rats. Concurrently, IoN ligation rats showed a limited increase in the responsiveness to stimulation of the contralateral IoN territory, and around postoperative days 30-40 the responsiveness to stimulation of facial areas outside the IoN territories also increased. The hyperresponsiveness to stimulation of the ligated IoN territory slightly decreased from 60 d postoperative. Throughout the study, IoN ligation rats showed decreased exploratory behavior, displayed more freezing-like behavior, had a slower body weight gain, and a higher defecation rate, compared to control rats. The behavioral alterations observed after CCI to the IoN are indicative of severe sensory disturbances within the territory of the injured nerve: mechanical allodynia develops after a period of relative hypo-/anesthesia during which behavioral signs of recurrent spontaneous, aversive (possibly painful) sensations (paresthesias/dysesthesias) are maximal.

0 comments Cited 115 times – based on 0 reviews      Review now

Bookmark

Record: found
Abstract: found
Article: not found

Fos expression in orexin neurons varies with behavioral state.

Ivy V Estabrooke, Marie T. McCarthy, Emily Ko … (2001)

The neuropeptide orexin (also known as hypocretin) is hypothesized to play a critical role in the regulation of sleep-wake behavior. Lack of orexin produces narcolepsy, which is characterized by poor maintenance of wakefulness and intrusions of rapid eye movement (REM) sleep or REM sleep-like phenomena into wakefulness. Orexin neurons heavily innervate many aminergic nuclei that promote wakefulness and inhibit REM sleep. We hypothesized that orexin neurons should be relatively active during wakefulness and inactive during sleep. To determine the pattern of activity of orexin neurons, we recorded sleep-wake behavior, body temperature, and locomotor activity under various conditions and used double-label immunohistochemistry to measure the expression of Fos in orexin neurons of the perifornical region. In rats maintained on a 12 hr light/dark cycle, more orexin neurons had Fos immunoreactive nuclei during the night period; in animals housed in constant darkness, this activation still occurred during the subjective night. Sleep deprivation or treatment with methamphetamine also increased Fos expression in orexin neurons. In each of these experiments, Fos expression in orexin neurons correlated positively with the amount of wakefulness and correlated negatively with the amounts of non-REM and REM sleep during the preceding 2 hr. In combination with previous work, these results suggest that activation of orexin neurons may contribute to the promotion or maintenance of wakefulness. Conversely, relative inactivity of orexin neurons may allow the expression of sleep.

0 comments Cited 93 times – based on 0 reviews      Review now

Bookmark

All references

Author and article information

Contributors

Seong Hoon Kim: antilefty4@gmail.com

Ju Yeon Park: pke1001@hanmail.net

Hae Eun Shin: alouet@hanmail.net

Si baek Lee: seeback.lee@gmail.com

Dong Woo Ryu: manrew@catholic.ac.kr

Tae Won Kim: kimtaewon79@gmail.com

Jeong Wook Park: +82-31-820-3575 , pjw5016@gmail.com

Journal

Journal ID (nlm-ta): J Headache Pain

Journal ID (iso-abbrev): J Headache Pain

Title: The Journal of Headache and Pain

Publisher: Springer Milan (Milan )

ISSN (Print): 1129-2369

ISSN (Electronic): 1129-2377

Publication date (Electronic): 1 March 2019

Publication date PMC-release: 1 March 2019

Publication date Collection: 2019

Volume: 20

Issue: 1

Electronic Location Identifier: 21

Affiliations

[1 ]ISNI 0000 0004 0647 8718, GRID grid.416981.3, Department of Neurology, , The Catholic University of Korea, College of Medicine, Uijeongbu St Mary’s Hospital, ; 65-1 Geumo-dong, Uijeongbu, Gyeonggi Do South Korea

[2 ]ISNI 0000 0004 0371 5685, GRID grid.464585.e, Department of Neurology, , The Catholic University of Korea, College of Medicine, Incheon St Mary’s Hospital, ; Incheon, South Korea

Article

Publisher ID: 977

DOI: 10.1186/s10194-019-0977-0

PMC ID: 6734525

PubMed ID: 30823867

SO-VID: 3fe5fb03-942a-4133-adb7-a5f660c34930

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.