Descending dopaminergic control of brainstem locomotor circuits

Fougère, Maxime; Flaive, Aurélie; Frigon, Alain; Ryczko, Dimitri

doi:10.1016/j.cophys.2018.12.004

Cited by 15 publications

(16 citation statements)

References 57 publications

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“…Fate mapping uncovered that these cholinergic neurons also express Vglut2 at one point during their lifetime (Steinkellner et al, 2019). Reciprocal connections exist between pedunculopontine cholinergic neurons and A9 (Lavoie & Parent, 1994; McGeer & McGeer, 1984; Ryczko et al, 2016; for review, Fougère, Flaive, Frigon, & Ryczko, 2019). Experimental destruction of each population leads to the degeneration of the other in a bidirectional manner (Bensaid, Michel, Clark, Hirsch, & François, 2016; Pienaar et al, 2015), suggesting that a transneuronal degeneration process occurs (Ryczko & Dubuc, 2017).…”

Section: Discussionmentioning

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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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: Discussionmentioning

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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“…TH staining was also observed in the arcuate nucleus and zona incerta, representing key nuclei of the hypothalamic tuberoinfundibular and incertohypothalamic dopaminergic pathways regulating prolactin secretion (Grattan, 2015) and locomotor activity (Fougère et al, 2019), respectively. Our results are in agreement with previous reports on TH expression determined by conventional 2D immunohistochemical (Araki et al, 2001; Bucci et al, 2017; D'Este et al, 2007; Jaber et al, 1999; Nelson et al, 1997; Ruggiero et al, 1984) and in situ mRNA hybridization techniques (Baker et al, 2003; Choi et al, 2012; Huang et al, 2005; Jakowec et al, 2004; Weiss-Wunder and Chesselet, 1991) (see …”

Section: Discussionmentioning

confidence: 99%

Quantitative whole-brain 3D imaging of tyrosine hydroxylase-labeled neuron architecture in the mouse MPTP model of Parkinson's disease

Roostalu

Salinas

Thorbek

et al. 2019

Disease Models &Amp; Mechanisms

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Parkinson's disease (PD) is a basal ganglia movement disorder characterized by progressive degeneration of the nigrostriatal dopaminergic system. Immunohistochemical methods have been widely used for characterization of dopaminergic neuronal injury in animal models of PD, including the MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) mouse model. However, conventional immunohistochemical techniques applied to tissue sections have inherent limitations with respect to loss of 3D resolution, yielding insufficient information on the architecture of the dopaminergic system. To provide a more comprehensive and non-biased map of MPTP-induced changes in central dopaminergic pathways, we used iDISCO immunolabeling, light-sheet fluorescence microscopy (LSFM) and deep-learning computational methods for whole-brain three-dimensional visualization and automated quantitation of tyrosine hydroxylase (TH)-positive neurons in the adult mouse brain. Mice terminated 7 days after acute MPTP administration demonstrated widespread alterations in TH expression. Compared to vehicle controls, MPTP-dosed mice showed a significant loss of TH-positive neurons in the substantia nigra pars compacta and ventral tegmental area. Also, MPTP dosing reduced overall TH signal intensity in basal ganglia nuclei, i.e. the substantia nigra, caudate-putamen, globus pallidus and subthalamic nucleus. In contrast, increased TH signal intensity was predominantly observed in limbic regions, including several subdivisions of the amygdala and hypothalamus. In conclusion, mouse whole-brain 3D imaging is ideal for unbiased automated counting and densitometric analysis of TH-positive cells. The LSFM–deep learning pipeline tracked brain-wide changes in catecholaminergic pathways in the MPTP mouse model of PD, and may be applied for preclinical characterization of compounds targeting dopaminergic neurotransmission.

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“…The MLR is under tonic inhibitory control of the output structures of the basal ganglia (Roseberry et al, 2016 ), which are involved in action selection, as well as planning and executing of gait modifications (Stephenson-Jones et al, 2011 ; Mullié et al, 2020 ; for review Grillner and Robertson, 2016 ). Dopaminergic nuclei influence the activity of the MLR indirectly through ascending projections to the basal ganglia (Kravitz et al, 2010 ), and directly through descending projections to the MLR (Ryczko et al, 2013 , 2016b ; Pérez-Fernández et al, 2014 ; Sharma et al, 2018 ), and the spinal cord (Koblinger et al, 2018 ; for review Fougère et al, 2019 ). The motor cortex is involved in precise foot placement by its projections to reticulospinal neurons and spinal CPG neurons (for review Drew and Marigold, 2015 ).…”

Section: The Locomotor Systemmentioning

confidence: 99%

Serotonergic Modulation of Locomotor Activity From Basal Vertebrates to Mammals

Flaive

Fougère

Zouwen

et al. 2020

Front. Neural Circuits

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During the last 50 years, the serotonergic (5-HT) system was reported to exert a complex modulation of locomotor activity. Here, we focus on two key factors that likely contribute to such complexity. First, locomotion is modulated directly and indirectly by 5-HT neurons. The locomotor circuitry is directly innervated by 5-HT neurons in the caudal brainstem and spinal cord. Also, indirect control of locomotor activity results from ascending projections of 5-HT cells in the rostral brainstem that innervate multiple brain centers involved in motor action planning. Second, each approach used to manipulate the 5-HT system likely engages different 5-HT-dependent mechanisms. This includes the recruitment of different 5-HT receptors, which can have excitatory or inhibitory effects on cell activity. These receptors can be located far or close to the 5-HT release sites, making their activation dependent on the level of 5-HT released. Here we review the activity of different 5-HT nuclei during locomotor activity, and the locomotor effects of 5-HT precursors, exogenous 5-HT, selective 5-HT reuptake inhibitors (SSRI), electrical or chemical stimulation of 5-HT neurons, genetic deletions, optogenetic and chemogenetic manipulations. We highlight both the coherent and controversial aspects of 5-HT modulation of locomotor activity from basal vertebrates to mammals. This mini review may hopefully inspire future studies aiming at dissecting the complex effects of 5-HT on locomotor function.

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Descending dopaminergic control of brainstem locomotor circuits

Cited by 15 publications

References 57 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

Quantitative whole-brain 3D imaging of tyrosine hydroxylase-labeled neuron architecture in the mouse MPTP model of Parkinson's disease

Serotonergic Modulation of Locomotor Activity From Basal Vertebrates to Mammals

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