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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

Analysis of individual zebrafish larval catecholaminergic neurons and projections in the context of the intact brain.(a) Scheme of dopaminergic (DA; blue) and noradrenergic (NA; red) cell groups and catecholaminergic (CA) tracts (grey) in 4 d.p.f. zebrafish larvae12. Left: lateral view of forebrain and midbrain; right: dorsal view of CNS. Dark blue indicates dorsal-most and light blue ventral-most DA groups. Diencephalic DA groups: (DC1) ventral thalamus and periventricular posterior tuberculum; (DC2, DC4) large neurons in posterior tuberculum; (DC5, DC6) medium-sized neurons in posterior tuberculum and hypothalamus; (DC3) medial hypothalamus; (DC7) caudal hypothalamus; PO, preoptic region; POa, anterior preoptic region; Pr, dorsal pretectum; AC, retinal amacrine cells. Telencephalic DA groups: SP, subpallium; OB, olfactory bulb. NA groups: LC, locus coeruleus; MO, medulla oblongata interfascicular zone and vagal area and AP, area postrema. ac, anterior commissure; act, anterior CA tract; eht, endohypothalamic tract; mlct, medial longitudinal CA tract; pc, posterior commissure; poc, postoptic commissure; poht, preopticohypothalamic tract; prp, pretectal projections; prtep, pretectotectal projections. (b–e) In silico separation of individual neurons (arrowheads in b) and their projections from whole-mount confocal image stack raw data. (b) Unprocessed maximum intensity projection (MIP) of a 4 d.p.f. larval brain. Blue masks D and L were manually drawn on the MIPs using ImageJ to separate soma and projections, based on visual discrimination. Bottom-most panel shows an example for computation of 3D segmentation mask M for a single neuron in the AP, based on the drawn masks D and L. The resulting 3D mask M was applied to the green channel to isolate the neuron and its projections. (c) Visualization of segmented AP neuron shown in (b) with projections. Quality control (QC; cyan) was carried out in 3D space within the region of interest (between dotted lines) to ensure the masks did not omit any GFP-labelled features belonging to the particular neuron. (d, e) Visualization of segmented individual soma and projections of GFP-labelled (d) amacrine cell (arrowheads) and (e) NA neuron in the MO interfasicular zone (IZ; arrowheads). See Supplementary Movie 1. Anterior at left, dorsal at top; anti-TH (red), anti-GFP (green); Dor, dorsal view; Lat, lateral view. Scale bars, 20 μm.
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f1: Analysis of individual zebrafish larval catecholaminergic neurons and projections in the context of the intact brain.(a) Scheme of dopaminergic (DA; blue) and noradrenergic (NA; red) cell groups and catecholaminergic (CA) tracts (grey) in 4 d.p.f. zebrafish larvae12. Left: lateral view of forebrain and midbrain; right: dorsal view of CNS. Dark blue indicates dorsal-most and light blue ventral-most DA groups. Diencephalic DA groups: (DC1) ventral thalamus and periventricular posterior tuberculum; (DC2, DC4) large neurons in posterior tuberculum; (DC5, DC6) medium-sized neurons in posterior tuberculum and hypothalamus; (DC3) medial hypothalamus; (DC7) caudal hypothalamus; PO, preoptic region; POa, anterior preoptic region; Pr, dorsal pretectum; AC, retinal amacrine cells. Telencephalic DA groups: SP, subpallium; OB, olfactory bulb. NA groups: LC, locus coeruleus; MO, medulla oblongata interfascicular zone and vagal area and AP, area postrema. ac, anterior commissure; act, anterior CA tract; eht, endohypothalamic tract; mlct, medial longitudinal CA tract; pc, posterior commissure; poc, postoptic commissure; poht, preopticohypothalamic tract; prp, pretectal projections; prtep, pretectotectal projections. (b–e) In silico separation of individual neurons (arrowheads in b) and their projections from whole-mount confocal image stack raw data. (b) Unprocessed maximum intensity projection (MIP) of a 4 d.p.f. larval brain. Blue masks D and L were manually drawn on the MIPs using ImageJ to separate soma and projections, based on visual discrimination. Bottom-most panel shows an example for computation of 3D segmentation mask M for a single neuron in the AP, based on the drawn masks D and L. The resulting 3D mask M was applied to the green channel to isolate the neuron and its projections. (c) Visualization of segmented AP neuron shown in (b) with projections. Quality control (QC; cyan) was carried out in 3D space within the region of interest (between dotted lines) to ensure the masks did not omit any GFP-labelled features belonging to the particular neuron. (d, e) Visualization of segmented individual soma and projections of GFP-labelled (d) amacrine cell (arrowheads) and (e) NA neuron in the MO interfasicular zone (IZ; arrowheads). See Supplementary Movie 1. Anterior at left, dorsal at top; anti-TH (red), anti-GFP (green); Dor, dorsal view; Lat, lateral view. Scale bars, 20 μm.

Mentions: We established an image analysis workflow to obtain a data set of single CA neuron projections and to identify and classify their projection behaviour (Fig. 1; Supplementary Methods, Supplementary Movie 1 and Supplementary Fig. S2). This imaging technique did not allow us to distinguish between axons and dendrites. Target area anatomical identities were confirmed from histological stains. To comprehensively analyse the CA projection network, we first dissected the characteristics of projections emanating from neurons of each CA group to include directionality (based on the body axes) and type (for example, arbourizing, branching, midline crossing, local; Supplementary Fig. S2). For further classification, major projections that are proximal to the cell soma and target the contralateral side were indicated as contralateral, whereas distal branches that originate from major ipsilateral projections but target contralaterally were documented as midline crossing processes. The second step was to visually trace all CA projections to their anatomical target areas (Fig. 2). Statistical analysis indicates that our data set is large enough to identify most (>80%) of the projection behaviours and target areas.


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)

Analysis of individual zebrafish larval catecholaminergic neurons and projections in the context of the intact brain.(a) Scheme of dopaminergic (DA; blue) and noradrenergic (NA; red) cell groups and catecholaminergic (CA) tracts (grey) in 4 d.p.f. zebrafish larvae12. Left: lateral view of forebrain and midbrain; right: dorsal view of CNS. Dark blue indicates dorsal-most and light blue ventral-most DA groups. Diencephalic DA groups: (DC1) ventral thalamus and periventricular posterior tuberculum; (DC2, DC4) large neurons in posterior tuberculum; (DC5, DC6) medium-sized neurons in posterior tuberculum and hypothalamus; (DC3) medial hypothalamus; (DC7) caudal hypothalamus; PO, preoptic region; POa, anterior preoptic region; Pr, dorsal pretectum; AC, retinal amacrine cells. Telencephalic DA groups: SP, subpallium; OB, olfactory bulb. NA groups: LC, locus coeruleus; MO, medulla oblongata interfascicular zone and vagal area and AP, area postrema. ac, anterior commissure; act, anterior CA tract; eht, endohypothalamic tract; mlct, medial longitudinal CA tract; pc, posterior commissure; poc, postoptic commissure; poht, preopticohypothalamic tract; prp, pretectal projections; prtep, pretectotectal projections. (b–e) In silico separation of individual neurons (arrowheads in b) and their projections from whole-mount confocal image stack raw data. (b) Unprocessed maximum intensity projection (MIP) of a 4 d.p.f. larval brain. Blue masks D and L were manually drawn on the MIPs using ImageJ to separate soma and projections, based on visual discrimination. Bottom-most panel shows an example for computation of 3D segmentation mask M for a single neuron in the AP, based on the drawn masks D and L. The resulting 3D mask M was applied to the green channel to isolate the neuron and its projections. (c) Visualization of segmented AP neuron shown in (b) with projections. Quality control (QC; cyan) was carried out in 3D space within the region of interest (between dotted lines) to ensure the masks did not omit any GFP-labelled features belonging to the particular neuron. (d, e) Visualization of segmented individual soma and projections of GFP-labelled (d) amacrine cell (arrowheads) and (e) NA neuron in the MO interfasicular zone (IZ; arrowheads). See Supplementary Movie 1. Anterior at left, dorsal at top; anti-TH (red), anti-GFP (green); Dor, dorsal view; Lat, lateral view. Scale bars, 20 μm.
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Related In: Results  -  Collection

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f1: Analysis of individual zebrafish larval catecholaminergic neurons and projections in the context of the intact brain.(a) Scheme of dopaminergic (DA; blue) and noradrenergic (NA; red) cell groups and catecholaminergic (CA) tracts (grey) in 4 d.p.f. zebrafish larvae12. Left: lateral view of forebrain and midbrain; right: dorsal view of CNS. Dark blue indicates dorsal-most and light blue ventral-most DA groups. Diencephalic DA groups: (DC1) ventral thalamus and periventricular posterior tuberculum; (DC2, DC4) large neurons in posterior tuberculum; (DC5, DC6) medium-sized neurons in posterior tuberculum and hypothalamus; (DC3) medial hypothalamus; (DC7) caudal hypothalamus; PO, preoptic region; POa, anterior preoptic region; Pr, dorsal pretectum; AC, retinal amacrine cells. Telencephalic DA groups: SP, subpallium; OB, olfactory bulb. NA groups: LC, locus coeruleus; MO, medulla oblongata interfascicular zone and vagal area and AP, area postrema. ac, anterior commissure; act, anterior CA tract; eht, endohypothalamic tract; mlct, medial longitudinal CA tract; pc, posterior commissure; poc, postoptic commissure; poht, preopticohypothalamic tract; prp, pretectal projections; prtep, pretectotectal projections. (b–e) In silico separation of individual neurons (arrowheads in b) and their projections from whole-mount confocal image stack raw data. (b) Unprocessed maximum intensity projection (MIP) of a 4 d.p.f. larval brain. Blue masks D and L were manually drawn on the MIPs using ImageJ to separate soma and projections, based on visual discrimination. Bottom-most panel shows an example for computation of 3D segmentation mask M for a single neuron in the AP, based on the drawn masks D and L. The resulting 3D mask M was applied to the green channel to isolate the neuron and its projections. (c) Visualization of segmented AP neuron shown in (b) with projections. Quality control (QC; cyan) was carried out in 3D space within the region of interest (between dotted lines) to ensure the masks did not omit any GFP-labelled features belonging to the particular neuron. (d, e) Visualization of segmented individual soma and projections of GFP-labelled (d) amacrine cell (arrowheads) and (e) NA neuron in the MO interfasicular zone (IZ; arrowheads). See Supplementary Movie 1. Anterior at left, dorsal at top; anti-TH (red), anti-GFP (green); Dor, dorsal view; Lat, lateral view. Scale bars, 20 μm.
Mentions: We established an image analysis workflow to obtain a data set of single CA neuron projections and to identify and classify their projection behaviour (Fig. 1; Supplementary Methods, Supplementary Movie 1 and Supplementary Fig. S2). This imaging technique did not allow us to distinguish between axons and dendrites. Target area anatomical identities were confirmed from histological stains. To comprehensively analyse the CA projection network, we first dissected the characteristics of projections emanating from neurons of each CA group to include directionality (based on the body axes) and type (for example, arbourizing, branching, midline crossing, local; Supplementary Fig. S2). For further classification, major projections that are proximal to the cell soma and target the contralateral side were indicated as contralateral, whereas distal branches that originate from major ipsilateral projections but target contralaterally were documented as midline crossing processes. The second step was to visually trace all CA projections to their anatomical target areas (Fig. 2). Statistical analysis indicates that our data set is large enough to identify most (>80%) of the projection behaviours and target areas.

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