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Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems.

Tay TL, Ronneberger O, Ryu S, Nitschke R, Driever W - Nat Commun (2011)

Bottom Line: The most extensive DA projections are established by posterior tubercular otp-dependent neurons, with individual somata integrating the ascending DA system, the descending diencephalospinal, as well as the endohypothalamic circuitry.We further identified an endogenous subpallial DA system that not only provides most of the local DA projections, but also connects to the ventral diencephalon.The catecholaminergic projectome map provides a framework to understand the evolution and function of these neuromodulatory systems.

View Article: PubMed Central - PubMed

Affiliation: Developmental Biology, Institute Biology I, Faculty of Biology, Albert-Ludwigs-University Freiburg, Hauptstrasse 1, Freiburg D-79104, Germany.

ABSTRACT
Essential components of animal behaviour are modulated by dopaminergic (DA) and noradrenergic circuitry. In this study, we reveal at cellular resolution the complete set of projections ('projectome') of every single type of DA and noradrenergio neurons in the central nervous system of zebrafish larvae. The most extensive DA projections are established by posterior tubercular otp-dependent neurons, with individual somata integrating the ascending DA system, the descending diencephalospinal, as well as the endohypothalamic circuitry. These findings suggest a major role in the modulation of physiology and behaviour for otp-dependent DA neurons, which correlate with the mammalian A11 group. We further identified an endogenous subpallial DA system that not only provides most of the local DA projections, but also connects to the ventral diencephalon. The catecholaminergic projectome map provides a framework to understand the evolution and function of these neuromodulatory systems.

No MeSH data available.


Related in: MedlinePlus

Individual somata of DC2 and DC4 emanate both ascending and descending projections.(a, b) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A DC2 neuron (arrowheads) within the posterior tuberculum (PT) projects both an ascending axon (single arrows) to the subpallium (SP) and a descending axon into the spinal cord. This neuron also forms a local arbour in the PT and ventral processes targeting the preoptic region (PO). Branches derived from the main descending axon were observed in the rhombencephalon (r), however, this region (double arrows) could not be clearly segmented because of the presence of a second GFP-labelled DC2 cell in the left PT, which contributed a midline-crossing branch into this area (inset). See Supplementary Movie 4. (b) A DC4 neuron (arrowheads) in the PT sends long ascending (single arrows) as well as descending (broad arrow) projections. Local processes in the PT and hypothalamus (H) also originate from this DC4 soma (double arrows). Its ascending projection arbourizes within the SP (magnified in the right panels). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (c) Schematic overview of DC2 and DC4 projection pathways (lines) and target areas (arrowheads). Dorsal (top) and lateral (bottom) views. 'L' denotes local arbours or processes. DC2 and DC4 neurons contribute to wide-ranging ipsilateral and contralateral projections into all major brain subdivisions. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. AP, area postrema; dl, lateral diencephalon; LC, locus coeruleus; MO, medulla oblongata; Pr, pretectum; T, tectum.
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f6: Individual somata of DC2 and DC4 emanate both ascending and descending projections.(a, b) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A DC2 neuron (arrowheads) within the posterior tuberculum (PT) projects both an ascending axon (single arrows) to the subpallium (SP) and a descending axon into the spinal cord. This neuron also forms a local arbour in the PT and ventral processes targeting the preoptic region (PO). Branches derived from the main descending axon were observed in the rhombencephalon (r), however, this region (double arrows) could not be clearly segmented because of the presence of a second GFP-labelled DC2 cell in the left PT, which contributed a midline-crossing branch into this area (inset). See Supplementary Movie 4. (b) A DC4 neuron (arrowheads) in the PT sends long ascending (single arrows) as well as descending (broad arrow) projections. Local processes in the PT and hypothalamus (H) also originate from this DC4 soma (double arrows). Its ascending projection arbourizes within the SP (magnified in the right panels). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (c) Schematic overview of DC2 and DC4 projection pathways (lines) and target areas (arrowheads). Dorsal (top) and lateral (bottom) views. 'L' denotes local arbours or processes. DC2 and DC4 neurons contribute to wide-ranging ipsilateral and contralateral projections into all major brain subdivisions. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. AP, area postrema; dl, lateral diencephalon; LC, locus coeruleus; MO, medulla oblongata; Pr, pretectum; T, tectum.

Mentions: Figure 2 summarizes projection patterns of all CA groups. Our further analysis structured the CA groups into five classes. First, NA systems comprise LC, MO vagal and AP neurons that share the main feature of far-ranging projections (Fig. 3), whereas NA neurons of the MO interfascicular zone predominantly connect locally (Supplementary Note 2 and Supplementary Fig. S3). The second class includes local as well as intermediate length projections of DA neurons: the larval DC1 group, which contains ventral thalamic and periventricular posterior tubercular DA neurons, and the pretectal DA group (Fig. 4; detailed in Supplementary Note 3). Class 3 DA groups project exclusively locally or to adjacent brain territories: hypothalamic anterior preoptic, preoptic, DC3 and DC7 groups, as well as olfactory and retinal DA groups (Fig. 4; Supplementary Note 4 and Fig. S4). In class 4, DA connections to distant brain regions appear to be predominantly formed by the otp-dependent diencephalic DA groups 2, 4, 5 and 6 (Figs 5, 6 and 7). Finally, in the subpallium local DA neurons provide the predominant DA arbourization as well as descending projections to the hypothalamus (Fig. 8).


Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems.

Tay TL, Ronneberger O, Ryu S, Nitschke R, Driever W - Nat Commun (2011)

Individual somata of DC2 and DC4 emanate both ascending and descending projections.(a, b) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A DC2 neuron (arrowheads) within the posterior tuberculum (PT) projects both an ascending axon (single arrows) to the subpallium (SP) and a descending axon into the spinal cord. This neuron also forms a local arbour in the PT and ventral processes targeting the preoptic region (PO). Branches derived from the main descending axon were observed in the rhombencephalon (r), however, this region (double arrows) could not be clearly segmented because of the presence of a second GFP-labelled DC2 cell in the left PT, which contributed a midline-crossing branch into this area (inset). See Supplementary Movie 4. (b) A DC4 neuron (arrowheads) in the PT sends long ascending (single arrows) as well as descending (broad arrow) projections. Local processes in the PT and hypothalamus (H) also originate from this DC4 soma (double arrows). Its ascending projection arbourizes within the SP (magnified in the right panels). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (c) Schematic overview of DC2 and DC4 projection pathways (lines) and target areas (arrowheads). Dorsal (top) and lateral (bottom) views. 'L' denotes local arbours or processes. DC2 and DC4 neurons contribute to wide-ranging ipsilateral and contralateral projections into all major brain subdivisions. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. AP, area postrema; dl, lateral diencephalon; LC, locus coeruleus; MO, medulla oblongata; Pr, pretectum; T, tectum.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3105308&req=5

f6: Individual somata of DC2 and DC4 emanate both ascending and descending projections.(a, b) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A DC2 neuron (arrowheads) within the posterior tuberculum (PT) projects both an ascending axon (single arrows) to the subpallium (SP) and a descending axon into the spinal cord. This neuron also forms a local arbour in the PT and ventral processes targeting the preoptic region (PO). Branches derived from the main descending axon were observed in the rhombencephalon (r), however, this region (double arrows) could not be clearly segmented because of the presence of a second GFP-labelled DC2 cell in the left PT, which contributed a midline-crossing branch into this area (inset). See Supplementary Movie 4. (b) A DC4 neuron (arrowheads) in the PT sends long ascending (single arrows) as well as descending (broad arrow) projections. Local processes in the PT and hypothalamus (H) also originate from this DC4 soma (double arrows). Its ascending projection arbourizes within the SP (magnified in the right panels). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (c) Schematic overview of DC2 and DC4 projection pathways (lines) and target areas (arrowheads). Dorsal (top) and lateral (bottom) views. 'L' denotes local arbours or processes. DC2 and DC4 neurons contribute to wide-ranging ipsilateral and contralateral projections into all major brain subdivisions. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. AP, area postrema; dl, lateral diencephalon; LC, locus coeruleus; MO, medulla oblongata; Pr, pretectum; T, tectum.
Mentions: Figure 2 summarizes projection patterns of all CA groups. Our further analysis structured the CA groups into five classes. First, NA systems comprise LC, MO vagal and AP neurons that share the main feature of far-ranging projections (Fig. 3), whereas NA neurons of the MO interfascicular zone predominantly connect locally (Supplementary Note 2 and Supplementary Fig. S3). The second class includes local as well as intermediate length projections of DA neurons: the larval DC1 group, which contains ventral thalamic and periventricular posterior tubercular DA neurons, and the pretectal DA group (Fig. 4; detailed in Supplementary Note 3). Class 3 DA groups project exclusively locally or to adjacent brain territories: hypothalamic anterior preoptic, preoptic, DC3 and DC7 groups, as well as olfactory and retinal DA groups (Fig. 4; Supplementary Note 4 and Fig. S4). In class 4, DA connections to distant brain regions appear to be predominantly formed by the otp-dependent diencephalic DA groups 2, 4, 5 and 6 (Figs 5, 6 and 7). Finally, in the subpallium local DA neurons provide the predominant DA arbourization as well as descending projections to the hypothalamus (Fig. 8).

Bottom Line: The most extensive DA projections are established by posterior tubercular otp-dependent neurons, with individual somata integrating the ascending DA system, the descending diencephalospinal, as well as the endohypothalamic circuitry.We further identified an endogenous subpallial DA system that not only provides most of the local DA projections, but also connects to the ventral diencephalon.The catecholaminergic projectome map provides a framework to understand the evolution and function of these neuromodulatory systems.

View Article: PubMed Central - PubMed

Affiliation: Developmental Biology, Institute Biology I, Faculty of Biology, Albert-Ludwigs-University Freiburg, Hauptstrasse 1, Freiburg D-79104, Germany.

ABSTRACT
Essential components of animal behaviour are modulated by dopaminergic (DA) and noradrenergic circuitry. In this study, we reveal at cellular resolution the complete set of projections ('projectome') of every single type of DA and noradrenergio neurons in the central nervous system of zebrafish larvae. The most extensive DA projections are established by posterior tubercular otp-dependent neurons, with individual somata integrating the ascending DA system, the descending diencephalospinal, as well as the endohypothalamic circuitry. These findings suggest a major role in the modulation of physiology and behaviour for otp-dependent DA neurons, which correlate with the mammalian A11 group. We further identified an endogenous subpallial DA system that not only provides most of the local DA projections, but also connects to the ventral diencephalon. The catecholaminergic projectome map provides a framework to understand the evolution and function of these neuromodulatory systems.

No MeSH data available.


Related in: MedlinePlus