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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

Projection behaviours of otp-dependent dopaminergic diencephalic clusters.(a–d) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. Lateral views correspond to magnified regions (middle panels). (a) A DC2 neuron (arrowheads) contributes to the endohypothalamic tract (eht), forms local arbours and ventral processes into preoptic region (PO) and hypothalamus (H) (magnified in middle panel). A long axon descends into the hindbrain with branches (arrows) across the midline, and into the spinal cord (not shown). (b) A DC4 soma (arrowheads) with short processes contributing to the eht and connecting within the hypothalamus (magnified in middle panel), a dorsal branch extending towards the lateral pretectum (Pr) and tectum (T) (bottom panel), and long descending axons (arrows) into left and right hindbrain. (c) A DC5 soma (arrowheads) with ipsilateral and contralateral contributions to the eht (magnified in middle panel). From the ipsilateral eht, a branch (arrow) extends dorsoposteriorly into the medial longitudinal catecholaminergic tract to the hindbrain. (d) A DC6 axon (arrowheads) arbourizes extensively in the hypothalamus (magnified in middle panel) and projects towards the caudal midbrain and anterior hindbrain (bottom panel). r, rhombencephalon. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (e) Schematic overview of DC2, DC4, DC5, and DC6 projection pathways (lines) and target areas (arrowheads) in lateral (left) and dorsal (right) views. 'L' denotes local arbours or processes. 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; PT, posterior tuberculum; SP, subpallium.
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f5: Projection behaviours of otp-dependent dopaminergic diencephalic clusters.(a–d) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. Lateral views correspond to magnified regions (middle panels). (a) A DC2 neuron (arrowheads) contributes to the endohypothalamic tract (eht), forms local arbours and ventral processes into preoptic region (PO) and hypothalamus (H) (magnified in middle panel). A long axon descends into the hindbrain with branches (arrows) across the midline, and into the spinal cord (not shown). (b) A DC4 soma (arrowheads) with short processes contributing to the eht and connecting within the hypothalamus (magnified in middle panel), a dorsal branch extending towards the lateral pretectum (Pr) and tectum (T) (bottom panel), and long descending axons (arrows) into left and right hindbrain. (c) A DC5 soma (arrowheads) with ipsilateral and contralateral contributions to the eht (magnified in middle panel). From the ipsilateral eht, a branch (arrow) extends dorsoposteriorly into the medial longitudinal catecholaminergic tract to the hindbrain. (d) A DC6 axon (arrowheads) arbourizes extensively in the hypothalamus (magnified in middle panel) and projects towards the caudal midbrain and anterior hindbrain (bottom panel). r, rhombencephalon. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (e) Schematic overview of DC2, DC4, DC5, and DC6 projection pathways (lines) and target areas (arrowheads) in lateral (left) and dorsal (right) views. 'L' denotes local arbours or processes. 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; PT, posterior tuberculum; SP, subpallium.

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)

Projection behaviours of otp-dependent dopaminergic diencephalic clusters.(a–d) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. Lateral views correspond to magnified regions (middle panels). (a) A DC2 neuron (arrowheads) contributes to the endohypothalamic tract (eht), forms local arbours and ventral processes into preoptic region (PO) and hypothalamus (H) (magnified in middle panel). A long axon descends into the hindbrain with branches (arrows) across the midline, and into the spinal cord (not shown). (b) A DC4 soma (arrowheads) with short processes contributing to the eht and connecting within the hypothalamus (magnified in middle panel), a dorsal branch extending towards the lateral pretectum (Pr) and tectum (T) (bottom panel), and long descending axons (arrows) into left and right hindbrain. (c) A DC5 soma (arrowheads) with ipsilateral and contralateral contributions to the eht (magnified in middle panel). From the ipsilateral eht, a branch (arrow) extends dorsoposteriorly into the medial longitudinal catecholaminergic tract to the hindbrain. (d) A DC6 axon (arrowheads) arbourizes extensively in the hypothalamus (magnified in middle panel) and projects towards the caudal midbrain and anterior hindbrain (bottom panel). r, rhombencephalon. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (e) Schematic overview of DC2, DC4, DC5, and DC6 projection pathways (lines) and target areas (arrowheads) in lateral (left) and dorsal (right) views. 'L' denotes local arbours or processes. 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; PT, posterior tuberculum; SP, subpallium.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: Projection behaviours of otp-dependent dopaminergic diencephalic clusters.(a–d) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. Lateral views correspond to magnified regions (middle panels). (a) A DC2 neuron (arrowheads) contributes to the endohypothalamic tract (eht), forms local arbours and ventral processes into preoptic region (PO) and hypothalamus (H) (magnified in middle panel). A long axon descends into the hindbrain with branches (arrows) across the midline, and into the spinal cord (not shown). (b) A DC4 soma (arrowheads) with short processes contributing to the eht and connecting within the hypothalamus (magnified in middle panel), a dorsal branch extending towards the lateral pretectum (Pr) and tectum (T) (bottom panel), and long descending axons (arrows) into left and right hindbrain. (c) A DC5 soma (arrowheads) with ipsilateral and contralateral contributions to the eht (magnified in middle panel). From the ipsilateral eht, a branch (arrow) extends dorsoposteriorly into the medial longitudinal catecholaminergic tract to the hindbrain. (d) A DC6 axon (arrowheads) arbourizes extensively in the hypothalamus (magnified in middle panel) and projects towards the caudal midbrain and anterior hindbrain (bottom panel). r, rhombencephalon. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (e) Schematic overview of DC2, DC4, DC5, and DC6 projection pathways (lines) and target areas (arrowheads) in lateral (left) and dorsal (right) views. 'L' denotes local arbours or processes. 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; PT, posterior tuberculum; SP, subpallium.
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