Characterization of glutamatergic VTA neural population responses to aversive and rewarding conditioning in freely-moving mice

Montardy, Quentin; Zhou, Zheng; Lei, Zhuogui; Liu, Xuemei; Zeng, Pengyu; Chen, Chen; Liu, Yuanming; Sanz‐Leon, Paula; Huang, Kang; Wang, Liping

doi:10.1016/j.scib.2019.05.005

Cited by 20 publications

(8 citation statements)

References 36 publications

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“…The Vglut2‐ire‐Cre mouse was used to study the role of hypothalamic neurons in feeding behavior (Liao, Kinney, An, & Xu, 2019; Rossi et al, 2019) or for deciphering the role of brainstem reticulospinal cells in locomotor control (Capelli, Pivetta, Soledad Esposito, & Arber, 2017). The same Vglut2‐ires‐Cre knock‐in allele is available on a mixed C57BL/6;FVB;129S6 genetic background and such mice were used to study the role of A10 Vglut2 neurons in the control of sleep and wakefulness (X. Yu, Li, et al 2019) and aversive and rewarding conditioning (Montardy et al, 2019) or to map the genes expressed by hypothalamic excitatory Vglut2‐positive neurons using single‐cell transcriptomics (Mickelsen et al, 2019) or to determine the Vglut2 expression in some cholinergic neurons and in some DA neurons in the brainstem using a fate mapping strategy (Steinkellner et al, 2018, 2019).…”

Section: Methodsmentioning

confidence: 99%

“…The same Vglut2-ires-Cre knock-in allele is available on a mixed C57BL/6; FVB;129S6 genetic background and such mice were used to study the role of A10 Vglut2 neurons in the control of sleep and wakefulness (X. Yu, Li, et al 2019) and aversive and rewarding conditioning (Montardy et al, 2019) or to map the genes expressed by hypothalamic excitatory Vglut2-positive neurons using single-cell transcriptomics (Mickelsen et al, 2019) or to determine the Vglut2 expression in some cholinergic neurons and in some DA neurons in the brainstem using a fate mapping strategy (Steinkellner et al, 2018(Steinkellner et al, , 2019.…”

Section: Specificity Of the Antibodiesmentioning

confidence: 99%

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Heterogeneous expression of dopaminergic markers and Vglut2 in mouse mesodiencephalic dopaminergic nuclei A8–A13

Fougère

Zouwen

Boutin

et al. 2020

J of Comparative Neurology

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Co-transmission of glutamate by brain dopaminergic (DA) neurons was recently proposed as a potential factor influencing cell survival in models of Parkinson's disease. Intriguingly, brain DA nuclei are differentially affected in Parkinson's disease. Whether this is associated with different patterns of co-expression of the glutamatergic phenotype along the rostrocaudal brain axis is unknown in mammals. We hypothesized that, as in zebrafish, the glutamatergic phenotype is present preferentially in the caudal mesodiencephalic DA nuclei. Here, we used in mice a cell fate mapping strategy based on reporter protein expression (ZsGreen) consecutive to previous expression of the vesicular glutamate transporter 2 (Vglut2) gene, coupled with immunofluorescence experiments against tyrosine hydroxylase (TH) or dopamine transporter (DAT). We found three expression patterns in DA cells, organized along the rostrocaudal brain axis. The first pattern (TH-positive, DAT-positive, ZsGreenpositive) was found in A8-A10. The second pattern (TH-positive, DAT-negative, ZsGreen-positive) was found in A11. The third pattern (TH-positive, DAT-negative, ZsGreen-negative) was found in A12-A13. These patterns should help to refine the establishment of the homology of DA nuclei between vertebrate species. Our results also uncover that Vglut2 is expressed at some point during cell lifetime in DA nuclei known to degenerate in Parkinson's disease and largely absent from those that are preserved, suggesting that co-expression of the glutamatergic phenotype in DA cells influences their survival in Parkinson's disease.

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Section: Methodsmentioning

confidence: 99%

Section: Specificity Of the Antibodiesmentioning

confidence: 99%

Heterogeneous expression of dopaminergic markers and Vglut2 in mouse mesodiencephalic dopaminergic nuclei A8–A13

Fougère

Zouwen

Boutin

et al. 2020

J of Comparative Neurology

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“…An alternative hypothesis is that different subpopulations of VTA glutamate neurons differentially drive reward and aversion through different mechanisms, similar to different projection-defined VTA DA sub-populations (de Jong et al, 2019). Indeed, initial investigations of VTA glutamate neuron activity in vivo shows a diversity of responses to salient rewarding and aversive stimuli (Montardy et al, 2019;Root et al, 2018b). Thus, one population of VTA glutamate neurons could drive approach through intra-VTA excitation of DA neurons, while another population may drive avoidance via projections to NAc or other distal structures.…”

Section: Reportmentioning

confidence: 99%

VTA Glutamate Neuron Activity Drives Positive Reinforcement Absent Dopamine Co-release

Zell

Steinkellner

Hollon

et al. 2020

Neuron

105

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“…Alternatively, the dPAG is also sending projections to structures such as the VTA [14]. Interestingly, VTA and dPAG glutamatergic neurons respond to aversive unconditioned and conditioned stimulation in a comparable manner [15]. Investigating dPAG to VTA function may help understanding the formation of aversive memory and emotion states.…”

Section: Conclusion and Discussionmentioning

confidence: 99%

Glutamatergic and GABAergic neuronal populations in the dorsolateral Periacqueductual Gray have different functional roles in fear conditioning

Montardy

Zhou

Liu

et al. 2019

Preprint

Self Cite

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It is though that only a subset of brain structures can encode emotional states. This can be investigated though a set of properties, including the ability of neurons to respond to a conditioned stimulus (CS) preceding an aversive unconditioned stimulus (US). The dorsolateral periacqueductal gray (dPAG) is a midbrain structure though to have an essential role in coordinating defensive behaviors in response to aversive stimulation. But its ability of dPAG neurons to encode a CS following fear conditioning as not been sufficiently studied.Here we used calcium imaging by fiber photometry to record the activity of dPAG VGluT2+ and dPAG GAD2+ neuronal populations during unconditioned and conditioned aversive stimulation. Then, following an unconditioned stimulation we performed a retrieval experiment to quantify memory-like responses of dPAG neurons. This shown that whilst both dPAG VGluT2+ and dPAG GAD2+ neuronal populations respond to direct US stimulation, and to CS stimulation during conditioning, only the dPAG VGluT2+ population persisted in responding to the CS stimulation during retrieval. Finally, to better understand dPAG VGluT2+ and dPAG GAD2+ connectivity patterns, we performed a cell specific monosynaptic retrograde rabies virus tracing experiment. This revealed that different patterns of fibers projects to dPAG VGluT2+ and dPAG GAD2+ , further complementing our recording showing divergences between PAG VGluT2+ and dPAG GAD2+ populations.

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Characterization of glutamatergic VTA neural population responses to aversive and rewarding conditioning in freely-moving mice

Cited by 20 publications

References 36 publications

Heterogeneous expression of dopaminergic markers and Vglut2 in mouse mesodiencephalic dopaminergic nuclei A8–A13

Heterogeneous expression of dopaminergic markers and Vglut2 in mouse mesodiencephalic dopaminergic nuclei A8–A13

VTA Glutamate Neuron Activity Drives Positive Reinforcement Absent Dopamine Co-release

Glutamatergic and GABAergic neuronal populations in the dorsolateral Periacqueductual Gray have different functional roles in fear conditioning

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