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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

Long-range projections of hindbrain noradrenergic neurons.(a–c) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A locus coeruleus noradrenergic (NA) neuron (arrowheads) projects into multiple regions of the brain including posterior tuberculum (PT), anterior preoptic region (POa) and the spinal cord (SC) via a descending branched axon. A projection from the soma ascends and crosses the midline via the posterior commissure (pc; arrow in middle bottom panel), and forms an arbour of fine processes within the tectum (T; magnified in rightmost panels). Middle and right panels are magnification of boxes in leftmost panels. See Supplementary Movie 2. H, hypothalamus. (b) A medulla oblongata vagal area (VA) NA neuron (arrowheads) sends a far-reaching axon into the tel- and diencephalon. The long axon forms branches within the posterior tuberculum to innervate the hypothalamus as well as the contralateral side via the anterior catecholaminergic tract (act) and the anterior commissure (ac). A short, branched process (top right panel) appears to target the rhombencephalon. Local fibres emanate from the proximal part of the axon. Middle and right panels are magnification of boxes in left panels. (c) A single area postrema (AP) NA soma (arrowheads) sends long ascending axons terminating in contra- and ipsilateral sides of the diencephalon. The right projection ends in the dorsal thalamus (THd), whereas the left innervates the preoptic region (PO; magnified in below dor and lat panels). See Supplementary Movie 3. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (d) Schematic overview of NA projections in 4 d.p.f. zebrafish larvae. Projection pathways (indicated by lines) and target areas (indicated by arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows (see MO and AP) denote formation of local arbours or processes. For visual clarity in dorsal views, lines and arrows are not depicted left–right reciprocally. Our data indicate no asymmetry. Ce, cerebellum; OB, olfactory bulb; P, pallium; poc, postoptic commissure; Pr, pretectum; SP, subpallium.
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f3: Long-range projections of hindbrain noradrenergic neurons.(a–c) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A locus coeruleus noradrenergic (NA) neuron (arrowheads) projects into multiple regions of the brain including posterior tuberculum (PT), anterior preoptic region (POa) and the spinal cord (SC) via a descending branched axon. A projection from the soma ascends and crosses the midline via the posterior commissure (pc; arrow in middle bottom panel), and forms an arbour of fine processes within the tectum (T; magnified in rightmost panels). Middle and right panels are magnification of boxes in leftmost panels. See Supplementary Movie 2. H, hypothalamus. (b) A medulla oblongata vagal area (VA) NA neuron (arrowheads) sends a far-reaching axon into the tel- and diencephalon. The long axon forms branches within the posterior tuberculum to innervate the hypothalamus as well as the contralateral side via the anterior catecholaminergic tract (act) and the anterior commissure (ac). A short, branched process (top right panel) appears to target the rhombencephalon. Local fibres emanate from the proximal part of the axon. Middle and right panels are magnification of boxes in left panels. (c) A single area postrema (AP) NA soma (arrowheads) sends long ascending axons terminating in contra- and ipsilateral sides of the diencephalon. The right projection ends in the dorsal thalamus (THd), whereas the left innervates the preoptic region (PO; magnified in below dor and lat panels). See Supplementary Movie 3. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (d) Schematic overview of NA projections in 4 d.p.f. zebrafish larvae. Projection pathways (indicated by lines) and target areas (indicated by arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows (see MO and AP) denote formation of local arbours or processes. For visual clarity in dorsal views, lines and arrows are not depicted left–right reciprocally. Our data indicate no asymmetry. Ce, cerebellum; OB, olfactory bulb; P, pallium; poc, postoptic commissure; Pr, pretectum; 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)

Long-range projections of hindbrain noradrenergic neurons.(a–c) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A locus coeruleus noradrenergic (NA) neuron (arrowheads) projects into multiple regions of the brain including posterior tuberculum (PT), anterior preoptic region (POa) and the spinal cord (SC) via a descending branched axon. A projection from the soma ascends and crosses the midline via the posterior commissure (pc; arrow in middle bottom panel), and forms an arbour of fine processes within the tectum (T; magnified in rightmost panels). Middle and right panels are magnification of boxes in leftmost panels. See Supplementary Movie 2. H, hypothalamus. (b) A medulla oblongata vagal area (VA) NA neuron (arrowheads) sends a far-reaching axon into the tel- and diencephalon. The long axon forms branches within the posterior tuberculum to innervate the hypothalamus as well as the contralateral side via the anterior catecholaminergic tract (act) and the anterior commissure (ac). A short, branched process (top right panel) appears to target the rhombencephalon. Local fibres emanate from the proximal part of the axon. Middle and right panels are magnification of boxes in left panels. (c) A single area postrema (AP) NA soma (arrowheads) sends long ascending axons terminating in contra- and ipsilateral sides of the diencephalon. The right projection ends in the dorsal thalamus (THd), whereas the left innervates the preoptic region (PO; magnified in below dor and lat panels). See Supplementary Movie 3. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (d) Schematic overview of NA projections in 4 d.p.f. zebrafish larvae. Projection pathways (indicated by lines) and target areas (indicated by arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows (see MO and AP) denote formation of local arbours or processes. For visual clarity in dorsal views, lines and arrows are not depicted left–right reciprocally. Our data indicate no asymmetry. Ce, cerebellum; OB, olfactory bulb; P, pallium; poc, postoptic commissure; Pr, pretectum; SP, subpallium.
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Related In: Results  -  Collection

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f3: Long-range projections of hindbrain noradrenergic neurons.(a–c) Z projections of confocal stacks in dorsal (Dor) and lateral (Lat) views. (a) A locus coeruleus noradrenergic (NA) neuron (arrowheads) projects into multiple regions of the brain including posterior tuberculum (PT), anterior preoptic region (POa) and the spinal cord (SC) via a descending branched axon. A projection from the soma ascends and crosses the midline via the posterior commissure (pc; arrow in middle bottom panel), and forms an arbour of fine processes within the tectum (T; magnified in rightmost panels). Middle and right panels are magnification of boxes in leftmost panels. See Supplementary Movie 2. H, hypothalamus. (b) A medulla oblongata vagal area (VA) NA neuron (arrowheads) sends a far-reaching axon into the tel- and diencephalon. The long axon forms branches within the posterior tuberculum to innervate the hypothalamus as well as the contralateral side via the anterior catecholaminergic tract (act) and the anterior commissure (ac). A short, branched process (top right panel) appears to target the rhombencephalon. Local fibres emanate from the proximal part of the axon. Middle and right panels are magnification of boxes in left panels. (c) A single area postrema (AP) NA soma (arrowheads) sends long ascending axons terminating in contra- and ipsilateral sides of the diencephalon. The right projection ends in the dorsal thalamus (THd), whereas the left innervates the preoptic region (PO; magnified in below dor and lat panels). See Supplementary Movie 3. Anterior at left, dorsal at top; 4 d.p.f. larvae; anti-TH (red), anti-GFP (green). Scale bars, 20 μm. (d) Schematic overview of NA projections in 4 d.p.f. zebrafish larvae. Projection pathways (indicated by lines) and target areas (indicated by arrowheads) are depicted in lateral (left) and dorsal (right) views. Short arrows (see MO and AP) denote formation of local arbours or processes. For visual clarity in dorsal views, lines and arrows are not depicted left–right reciprocally. Our data indicate no asymmetry. Ce, cerebellum; OB, olfactory bulb; P, pallium; poc, postoptic commissure; Pr, pretectum; 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