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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

Dopaminergic groups with characteristic short-range or local projection behaviours.(a–e) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A pretectal dopaminergic (DA) neuron (arrowheads) forms a local arbour within the pretectum (Pr) and projects into the ipsilateral tectum (T; magnified in right panel) and across the posterior commissure (pc) to the contralateral tectum (left panel). H, hypothalamus. (b) A diencephalic cluster (DC) 1 neuron (arrowheads) sends short proximal processes within the ventral thalamus (THv), into the endohypothalamic tract (eht) (magnified in middle and rightmost panels), and descending projections into the rhombencephalon (r). (c) A preoptic DA neuron (arrowhead) projects into the postoptic commissure (poc) and eht (magnified in right panel). (d) A DC3 neuron (arrowhead) located in the paraventricular organ (PVO) is liquor contacting (arrows pointing to end-foot) and contributes to the eht and hypothalamus (magnified in right panel; inset shows GFP signal). (e) Liquor-contacting DC7 soma (arrowhead) within the posterior recess possesses sparse processes (magnified in right panel) that target locally in the caudal hypothalamus (Hc). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green, white in panels with black contrast). Scale bars, 20 μm. (f) Scheme of DA groups with local and intermediate projections (4 d.p.f.). Projection pathways (lines) and target areas (arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows and 'L' denote local arbours or processes. An asterisk (*) marks liquor-contacting DA groups. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. ac, anterior commissure; AP, area postrema; LC, locus coeruleus; and MO, medulla oblongata.
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f4: Dopaminergic groups with characteristic short-range or local projection behaviours.(a–e) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A pretectal dopaminergic (DA) neuron (arrowheads) forms a local arbour within the pretectum (Pr) and projects into the ipsilateral tectum (T; magnified in right panel) and across the posterior commissure (pc) to the contralateral tectum (left panel). H, hypothalamus. (b) A diencephalic cluster (DC) 1 neuron (arrowheads) sends short proximal processes within the ventral thalamus (THv), into the endohypothalamic tract (eht) (magnified in middle and rightmost panels), and descending projections into the rhombencephalon (r). (c) A preoptic DA neuron (arrowhead) projects into the postoptic commissure (poc) and eht (magnified in right panel). (d) A DC3 neuron (arrowhead) located in the paraventricular organ (PVO) is liquor contacting (arrows pointing to end-foot) and contributes to the eht and hypothalamus (magnified in right panel; inset shows GFP signal). (e) Liquor-contacting DC7 soma (arrowhead) within the posterior recess possesses sparse processes (magnified in right panel) that target locally in the caudal hypothalamus (Hc). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green, white in panels with black contrast). Scale bars, 20 μm. (f) Scheme of DA groups with local and intermediate projections (4 d.p.f.). Projection pathways (lines) and target areas (arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows and 'L' denote local arbours or processes. An asterisk (*) marks liquor-contacting DA groups. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. ac, anterior commissure; AP, area postrema; LC, locus coeruleus; and MO, medulla oblongata.

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)

Dopaminergic groups with characteristic short-range or local projection behaviours.(a–e) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A pretectal dopaminergic (DA) neuron (arrowheads) forms a local arbour within the pretectum (Pr) and projects into the ipsilateral tectum (T; magnified in right panel) and across the posterior commissure (pc) to the contralateral tectum (left panel). H, hypothalamus. (b) A diencephalic cluster (DC) 1 neuron (arrowheads) sends short proximal processes within the ventral thalamus (THv), into the endohypothalamic tract (eht) (magnified in middle and rightmost panels), and descending projections into the rhombencephalon (r). (c) A preoptic DA neuron (arrowhead) projects into the postoptic commissure (poc) and eht (magnified in right panel). (d) A DC3 neuron (arrowhead) located in the paraventricular organ (PVO) is liquor contacting (arrows pointing to end-foot) and contributes to the eht and hypothalamus (magnified in right panel; inset shows GFP signal). (e) Liquor-contacting DC7 soma (arrowhead) within the posterior recess possesses sparse processes (magnified in right panel) that target locally in the caudal hypothalamus (Hc). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green, white in panels with black contrast). Scale bars, 20 μm. (f) Scheme of DA groups with local and intermediate projections (4 d.p.f.). Projection pathways (lines) and target areas (arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows and 'L' denote local arbours or processes. An asterisk (*) marks liquor-contacting DA groups. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. ac, anterior commissure; AP, area postrema; LC, locus coeruleus; and MO, medulla oblongata.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f4: Dopaminergic groups with characteristic short-range or local projection behaviours.(a–e) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A pretectal dopaminergic (DA) neuron (arrowheads) forms a local arbour within the pretectum (Pr) and projects into the ipsilateral tectum (T; magnified in right panel) and across the posterior commissure (pc) to the contralateral tectum (left panel). H, hypothalamus. (b) A diencephalic cluster (DC) 1 neuron (arrowheads) sends short proximal processes within the ventral thalamus (THv), into the endohypothalamic tract (eht) (magnified in middle and rightmost panels), and descending projections into the rhombencephalon (r). (c) A preoptic DA neuron (arrowhead) projects into the postoptic commissure (poc) and eht (magnified in right panel). (d) A DC3 neuron (arrowhead) located in the paraventricular organ (PVO) is liquor contacting (arrows pointing to end-foot) and contributes to the eht and hypothalamus (magnified in right panel; inset shows GFP signal). (e) Liquor-contacting DC7 soma (arrowhead) within the posterior recess possesses sparse processes (magnified in right panel) that target locally in the caudal hypothalamus (Hc). Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green, white in panels with black contrast). Scale bars, 20 μm. (f) Scheme of DA groups with local and intermediate projections (4 d.p.f.). Projection pathways (lines) and target areas (arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows and 'L' denote local arbours or processes. An asterisk (*) marks liquor-contacting DA groups. For visual clarity, lines and arrows are not depicted left–right reciprocally in dorsal views. Our data indicate no asymmetry. ac, anterior commissure; AP, area postrema; LC, locus coeruleus; and MO, medulla oblongata.
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