Superior Colliculus GABAergic Neurons Are Essential for Acute Dark Induction of Wakefulness in Mice

Zhang, Ze; Liu, Wenying; Diao, Yupu; Xu, Wei; Zhong, Yuan; Zhang, Jiayi; Lazarus, Michael; Liu, Yuan-Yuan; Qu, Wei‐Min; Huang, Zhi‐Li

doi:10.1016/j.cub.2018.12.031

Cited by 59 publications

(61 citation statements)

References 40 publications

(51 reference statements)

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“…Neurons that did not satisfy these criteria were identified as TH− neurons ( Supplementary Fig. 5j), as previously described [12,25,56,57].…”

Section: In Vitro Electrophysiologymentioning

confidence: 99%

Ventral pallidal GABAergic neurons control wakefulness associated with motivation through the ventral tegmental pathway

Luo

et al. 2020

Mol Psychiatry

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The ventral pallidum (VP) regulates motivation, drug addiction, and several behaviors that rely on heightened arousal. However, the role and underlying neural circuits of the VP in the control of wakefulness remain poorly understood. In the present study, we sought to elucidate the specific role of VP GABAergic neurons in controlling sleep–wake behaviors in mice. Fiber photometry revealed that the population activity of VP GABAergic neurons was increased during physiological transitions from non-rapid eye movement (non-REM, NREM) sleep to either wakefulness or REM sleep. Moreover, chemogenetic and optogenetic manipulations were leveraged to investigate a potential causal role of VP GABAergic neurons in initiating and/or maintaining arousal. In vivo optogenetic stimulation of VP GABAergic neurons innervating the ventral tegmental area (VTA) strongly promoted arousal via disinhibition of VTA dopaminergic neurons. Functional in vitro mapping revealed that VP GABAergic neurons, in principle, inhibited VTA GABAergic neurons but also inhibited VTA dopaminergic neurons. In addition, optogenetic stimulation of terminals of VP GABAergic neurons revealed that they promoted arousal by innervating the lateral hypothalamus, but not the mediodorsal thalamus or lateral habenula. The increased wakefulness chemogenetically evoked by VP GABAergic neuronal activation was completely abolished by pretreatment with dopaminergic D1 and D2/D3 receptor antagonists. Furthermore, activation of VP GABAergic neurons increased exploration time in both the open-field and light–dark box tests but did not modulate depression-like behaviors or food intake. Finally, chemogenetic inhibition of VP GABAergic neurons decreased arousal. Taken together, our findings indicate that VP GABAergic neurons are essential for arousal related to motivation.

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“…Neurons that did not satisfy these criteria were identified as TH− neurons ( Supplementary Fig. 5j), as previously described [12,25,56,57].…”

Section: In Vitro Electrophysiologymentioning

confidence: 99%

Ventral pallidal GABAergic neurons control wakefulness associated with motivation through the ventral tegmental pathway

Luo

et al. 2020

Mol Psychiatry

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“…While the function of some SC neurons have been studied during behavior [23][24][25][26] ,characterization of GABAergic neurons in the intermediate and deep layers has primarily been limited to anatomy and slice physiology 33,34,38,49 . We have identified a functional role for these neurons in mediating spatial choice via intercollicular inhibition ( Fig.…”

Section: Discussionmentioning

confidence: 99%

“…These and other data showing that SC activity reflects target value and other decision-related variables 12,21,22 demonstrate that the SC, traditionally appreciated for initiating orienting motor commands, is required for choosing where to move 7 . While the SC has recently served as an exquisite experimental system for probing neural circuit function in multiple behavioral contexts [23][24][25][26] , how SC circuits mediate spatial choice remains unclear.…”

Section: Introductionmentioning

confidence: 99%

Inhibitory midbrain neurons mediate decision making

Essig

Hunt

Felsen

2020

Preprint

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Decision making is critical for survival but its neural basis is unclear. Here we examine how functional neural circuitry in the output layers of the midbrain superior colliculus (SC) mediates spatial choice, an SC-dependent tractable form of decision making. We focus on the role of inhibitory SC neurons, using optogenetics to record and manipulate their activity in behaving mice. Based on data from SC slice experiments and on a canonical role of inhibitory neurons in cortical microcircuits, we hypothesized that inhibitory SC neurons locally inhibit premotor output neurons that represent contralateral targets. However, our experimental results refuted this hypothesis. An attractor model revealed that our results were instead consistent with inhibitory neurons providing long-range inhibition between the two SCs, and terminal activation experiments supported this architecture. Our study provides mechanistic evidence for competitive inhibition between populations representing discrete choices, a common motif in theoretical models of decision making.

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“…In nocturnal rodents, the SC has been shown to be critical for maintaining sleep when the lights are on (Miller et al, 1998). It has been recently shown that GABAergic neurons in the SC are critical for inducing wakefulness when the lights are off (Zhang et al, 2019). In addition, light input is critical for the SC to develop properly (Prichard et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

Superior Colliculus Lesions Lead to Disrupted Responses to Light in Diurnal Grass Rats (Arvicanthis niloticus)

et al. 2019

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The circadian system regulates daily rhythms of physiology and behavior. Although extraordinary advances have been made to elucidate the brain mechanisms underlying the circadian system in nocturnal species, less is known in diurnal species. Recent studies have shown that retinorecipient brain areas such as the intergeniculate leaflet (IGL) and olivary pretectal nucleus (OPT) are critical for the display of normal patterns of daily activity in diurnal grass rats ( Arvicanthis niloticus). Specifically, grass rats with IGL and OPT lesions respond to light in similar ways to intact nocturnal animals. Importantly, both the IGL and OPT project to one another in nocturnal species, and there is evidence that these 2 brain regions also project to the superior colliculus (SC). The SC receives direct retinal input, is involved in the triggering of rapid eye movement sleep in nocturnal rats, and is disproportionately large in the diurnal grass rat. The objective of the current study was to use diurnal grass rats to test the hypothesis that the SC is critical for the expression of diurnal behavior and physiology. We performed bilateral electrolytic lesions of the SC in female grass rats to examine behavioral patterns and acute responses to light. Most grass rats with SC lesions expressed significantly reduced activity in the presence of light. Exposing these grass rats to constant darkness reinstated activity levels during the subjective day, suggesting that light masks their ability to display a diurnal activity profile in 12:12 LD. Altogether, our data suggest that the SC is critical for maintaining normal responses to light in female grass rats.

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Superior Colliculus GABAergic Neurons Are Essential for Acute Dark Induction of Wakefulness in Mice

Cited by 59 publications

References 40 publications

Ventral pallidal GABAergic neurons control wakefulness associated with motivation through the ventral tegmental pathway

Ventral pallidal GABAergic neurons control wakefulness associated with motivation through the ventral tegmental pathway

Inhibitory midbrain neurons mediate decision making

Superior Colliculus Lesions Lead to Disrupted Responses to Light in Diurnal Grass Rats (Arvicanthis niloticus)

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