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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

Diversity of projection behaviour subtypes of individual DC2 and DC4 neurons.DA neurons of one anatomical group express high diversity of projection behaviours within defined repertoires. DC2 (69 somata) and DC4 (42 somata) neurons were analysed and shown to connect to tel-, di-, mes- and rhombencephalon. Individual somata usually connect through the endohypothalamic tract and send different combinations of projections to the subpallium, lateral forebrain, lateral tectum, hindbrain and/or spinal cord. DA innervation in the preoptic region and lateral forebrain primarily derives from DC2 cells. Individual somata were classified on the basis of their major projections (green), but smaller deviations in branching pattern and targets were allowed (yellow and light green). The rightmost column indicates the number of cells observed for each specific pattern (rows), and in parentheses the total number of cells analysed for DC2 and DC4. Dor, dorsal projections; lat, lateral projections; single in endohypothalamic tract indicates contribution of single axon to tract; (#) ipsilateral distal branch that crosses the midline to target the contralateral side.
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f7: Diversity of projection behaviour subtypes of individual DC2 and DC4 neurons.DA neurons of one anatomical group express high diversity of projection behaviours within defined repertoires. DC2 (69 somata) and DC4 (42 somata) neurons were analysed and shown to connect to tel-, di-, mes- and rhombencephalon. Individual somata usually connect through the endohypothalamic tract and send different combinations of projections to the subpallium, lateral forebrain, lateral tectum, hindbrain and/or spinal cord. DA innervation in the preoptic region and lateral forebrain primarily derives from DC2 cells. Individual somata were classified on the basis of their major projections (green), but smaller deviations in branching pattern and targets were allowed (yellow and light green). The rightmost column indicates the number of cells observed for each specific pattern (rows), and in parentheses the total number of cells analysed for DC2 and DC4. Dor, dorsal projections; lat, lateral projections; single in endohypothalamic tract indicates contribution of single axon to tract; (#) ipsilateral distal branch that crosses the midline to target the contralateral side.

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)

Diversity of projection behaviour subtypes of individual DC2 and DC4 neurons.DA neurons of one anatomical group express high diversity of projection behaviours within defined repertoires. DC2 (69 somata) and DC4 (42 somata) neurons were analysed and shown to connect to tel-, di-, mes- and rhombencephalon. Individual somata usually connect through the endohypothalamic tract and send different combinations of projections to the subpallium, lateral forebrain, lateral tectum, hindbrain and/or spinal cord. DA innervation in the preoptic region and lateral forebrain primarily derives from DC2 cells. Individual somata were classified on the basis of their major projections (green), but smaller deviations in branching pattern and targets were allowed (yellow and light green). The rightmost column indicates the number of cells observed for each specific pattern (rows), and in parentheses the total number of cells analysed for DC2 and DC4. Dor, dorsal projections; lat, lateral projections; single in endohypothalamic tract indicates contribution of single axon to tract; (#) ipsilateral distal branch that crosses the midline to target the contralateral side.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f7: Diversity of projection behaviour subtypes of individual DC2 and DC4 neurons.DA neurons of one anatomical group express high diversity of projection behaviours within defined repertoires. DC2 (69 somata) and DC4 (42 somata) neurons were analysed and shown to connect to tel-, di-, mes- and rhombencephalon. Individual somata usually connect through the endohypothalamic tract and send different combinations of projections to the subpallium, lateral forebrain, lateral tectum, hindbrain and/or spinal cord. DA innervation in the preoptic region and lateral forebrain primarily derives from DC2 cells. Individual somata were classified on the basis of their major projections (green), but smaller deviations in branching pattern and targets were allowed (yellow and light green). The rightmost column indicates the number of cells observed for each specific pattern (rows), and in parentheses the total number of cells analysed for DC2 and DC4. Dor, dorsal projections; lat, lateral projections; single in endohypothalamic tract indicates contribution of single axon to tract; (#) ipsilateral distal branch that crosses the midline to target the contralateral side.
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