Dorsal Raphe Dopamine Neurons Modulate Arousal and Promote Wakefulness by Salient Stimuli

Ventral midbrain dopamine (DA) is unambiguously involved in motivation and behavioral arousal, yet the contributions of other DA populations to these processes are poorly understood. Here, we demonstrate that the dorsal raphe nucleus DA neurons are critical modulators of behavioral arousal and sleep...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2017-06, Vol.94 (6), p.1205-1219.e8
Main Authors: Cho, Jounhong Ryan, Treweek, Jennifer B., Robinson, J. Elliott, Xiao, Cheng, Bremner, Lindsay R., Greenbaum, Alon, Gradinaru, Viviana
Format: Article
Language:English
Subjects:
Animals
Arousal
Arousal - physiology
chemogenetics
Cues
Dopamine
Dopamine receptors
Dopaminergic Neurons - cytology
Dopaminergic Neurons - physiology
Dorsal raphe nucleus
Dorsal Raphe Nucleus - cytology
Dorsal Raphe Nucleus - physiology
Electroencephalography
Electromyography
fiber photometry
Hindlimb Suspension
in vivo optical imaging during behavior
Mesencephalon
Mice
Motivation
Neuromodulation
Neurons
Neurosciences
NREM sleep
Optical Imaging
Optogenetics
Photometry
Population
Raphe nuclei
Restraint, Physical
Rodents
salience
Signal strength
Sleep
Sleep - physiology
Sleep and wakefulness
Sleep, REM
sleep-wake state
ventral periaqueductal gray
Vigilance
Wakefulness
Wakefulness - physiology
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Summary:Ventral midbrain dopamine (DA) is unambiguously involved in motivation and behavioral arousal, yet the contributions of other DA populations to these processes are poorly understood. Here, we demonstrate that the dorsal raphe nucleus DA neurons are critical modulators of behavioral arousal and sleep-wake patterning. Using simultaneous fiber photometry and polysomnography, we observed time-delineated dorsal raphe nucleus dopaminergic (DRNDA) activity upon exposure to arousal-evoking salient cues, irrespective of their hedonic valence. We also observed broader fluctuations of DRNDA activity across sleep-wake cycles with highest activity during wakefulness. Both endogenous DRNDA activity and optogenetically driven DRNDA activity were associated with waking from sleep, with DA signal strength predictive of wake duration. Conversely, chemogenetic inhibition opposed wakefulness and promoted NREM sleep, even in the face of salient stimuli. Therefore, the DRNDA population is a critical contributor to wake-promoting pathways and is capable of modulating sleep-wake states according to the outside environment, wherein the perception of salient stimuli prompts vigilance and arousal. •DRNDA neurons are activated by salient stimuli irrespective of hedonic valence•DRNDA activity fluctuates across sleep-wake states and is highest at wakefulness•Optogenetic activation promotes wakefulness•Chemogenetic inhibition opposes wakefulness, even in the presence of salient stimuli Cho et al. demonstrate that dorsal raphe nucleus dopaminergic (DRNDA) activity escalates in response to salient stimuli irrespective of valence, correlates with sleep-wake states, and can bi-directionally modulate arousal.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2017.05.020