Chemogenetic inhibition of the medial prefrontal cortex reverses the effects of REM sleep loss on sucrose consumption

Kristopher McEown; Yohko Takata; Yoan Cherasse; Nanae Nagata; Kosuke Aritake; Michael Lazarus

doi:10.7554/eLife.20269

Chemogenetic inhibition of the medial prefrontal cortex reverses the effects of REM sleep loss on sucrose consumption

Kristopher McEown, Yohko Takata, Yoan Cherasse, Nanae Nagata, Kosuke Aritake, Michael Lazarus^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

8 Citations (Scopus)

Abstract

Rapid eye movement (REM) sleep loss is associated with increased consumption of weight-promoting foods. The prefrontal cortex (PFC) is thought to mediate reward anticipation. However, the precise role of the PFC in mediating reward responses to highly palatable foods (HPF) after REM sleep deprivation is unclear. We selectively reduced REM sleep in mice over a 25-48 hr period and chemogenetically inhibited the medial PFC (mPFC) by using an altered glutamategated and ivermectin-gated chloride channel that facilitated neuronal inhibition through hyperpolarizing infected neurons. HPF consumption was measured while the mPFC was inactivated and REM sleep loss was induced. We found that REM sleep loss increased HPF consumption compared to control animals. However, mPFC inactivation reversed the effect of REM sleep loss on sucrose consumption without affecting fat consumption. Our findings provide, for the first time, a causal link between REM sleep, mPFC function and HPF consumption.

Original language	English
Article number	e20269
Journal	eLife
Volume	5
Issue number	DECEMBER2016
DOIs	https://doi.org/10.7554/eLife.20269
Publication status	Published - 2016 Dec 6
Externally published	Yes

ASJC Scopus subject areas

Neuroscience(all)
Immunology and Microbiology(all)
Biochemistry, Genetics and Molecular Biology(all)

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10.7554/eLife.20269

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title = "Chemogenetic inhibition of the medial prefrontal cortex reverses the effects of REM sleep loss on sucrose consumption",

abstract = "Rapid eye movement (REM) sleep loss is associated with increased consumption of weight-promoting foods. The prefrontal cortex (PFC) is thought to mediate reward anticipation. However, the precise role of the PFC in mediating reward responses to highly palatable foods (HPF) after REM sleep deprivation is unclear. We selectively reduced REM sleep in mice over a 25-48 hr period and chemogenetically inhibited the medial PFC (mPFC) by using an altered glutamategated and ivermectin-gated chloride channel that facilitated neuronal inhibition through hyperpolarizing infected neurons. HPF consumption was measured while the mPFC was inactivated and REM sleep loss was induced. We found that REM sleep loss increased HPF consumption compared to control animals. However, mPFC inactivation reversed the effect of REM sleep loss on sucrose consumption without affecting fat consumption. Our findings provide, for the first time, a causal link between REM sleep, mPFC function and HPF consumption.",

author = "Kristopher McEown and Yohko Takata and Yoan Cherasse and Nanae Nagata and Kosuke Aritake and Michael Lazarus",

note = "Funding Information: This work was supported by a Japan Society for the Promotion of Science KAKENHI grant (2604762, to ML) and postdoctoral fellowship (P14762, to KM); a Takeda Science Foundation postdoctoral fellowship (to KM); a grant from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan (Grant-in-Aid for Scientific Research on Innovative Areas ?Living in Space?, 16H01629, to ML); a CREST grant from the Japan Science and Technology Agency (to ML) and the World Premier International Research Center Initiative (WPI) from MEXT (to ML, YT, YC, NN and KA). Japan Society for the Promotion of Science P14762 Kristopher McEown Japan Society for the Promotion of Science 2604762 Michael Lazarus Ministry of Education, Culture, Sports, Science, and Technology 16H01629 Michael Lazarus Japan Science and Technology Agency 16814578 Michael Lazarus The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: {\textcopyright} McEown et al.",

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AU - Takata, Yohko

AU - Cherasse, Yoan

AU - Nagata, Nanae

AU - Aritake, Kosuke

AU - Lazarus, Michael

N1 - Funding Information: This work was supported by a Japan Society for the Promotion of Science KAKENHI grant (2604762, to ML) and postdoctoral fellowship (P14762, to KM); a Takeda Science Foundation postdoctoral fellowship (to KM); a grant from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan (Grant-in-Aid for Scientific Research on Innovative Areas ?Living in Space?, 16H01629, to ML); a CREST grant from the Japan Science and Technology Agency (to ML) and the World Premier International Research Center Initiative (WPI) from MEXT (to ML, YT, YC, NN and KA). Japan Society for the Promotion of Science P14762 Kristopher McEown Japan Society for the Promotion of Science 2604762 Michael Lazarus Ministry of Education, Culture, Sports, Science, and Technology 16H01629 Michael Lazarus Japan Science and Technology Agency 16814578 Michael Lazarus The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Publisher Copyright: © McEown et al.

PY - 2016/12/6

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N2 - Rapid eye movement (REM) sleep loss is associated with increased consumption of weight-promoting foods. The prefrontal cortex (PFC) is thought to mediate reward anticipation. However, the precise role of the PFC in mediating reward responses to highly palatable foods (HPF) after REM sleep deprivation is unclear. We selectively reduced REM sleep in mice over a 25-48 hr period and chemogenetically inhibited the medial PFC (mPFC) by using an altered glutamategated and ivermectin-gated chloride channel that facilitated neuronal inhibition through hyperpolarizing infected neurons. HPF consumption was measured while the mPFC was inactivated and REM sleep loss was induced. We found that REM sleep loss increased HPF consumption compared to control animals. However, mPFC inactivation reversed the effect of REM sleep loss on sucrose consumption without affecting fat consumption. Our findings provide, for the first time, a causal link between REM sleep, mPFC function and HPF consumption.

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Chemogenetic inhibition of the medial prefrontal cortex reverses the effects of REM sleep loss on sucrose consumption

Abstract

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