Expression of the paralogous tyrosine hydroxylase encoding genes th1 and th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain

Alida Filippi,Jörn Schweitzer,Wolfgang Driever,Julia Mahler

doi:10.1002/cne.22213

Alida Filippi, Jörn Schweitzer + Show 2 more

Open Access

https://doi.org/10.1002/cne.22213

Copy DOI

Abstract

The development of dopaminergic and noradrenergic neurons has received much attention based on their modulatory effect on many behavioral circuits and their involvement in neurodegenerative diseases. The zebrafish (Danio rerio) has emerged as a new model organism with which to study development and function of catecholaminergic systems. Tyrosine hydroxylase is the entry enzyme into catecholamine biosynthesis and is frequently used as a marker for catecholaminergic neurons. A genome duplication at the base of teleost evolution resulted in two paralogous zebrafish tyrosine hydroxylase-encoding genes, th1 and th2, the expression of which has been described previously only for th1. Here we investigate the expression of th2 in the brain of embryonic and juvenile zebrafish. We optimized whole-mount in situ hybridization protocols to detect gene expression in the anatomical three-dimensional context of whole juvenile brains. To confirm whether th2-expressing cells may indeed use dopamine as a neurotransmitter, we also included expression of dopamine beta hydroxylase, dopa decarboxylase, and dopamine transporter in our analysis. Our data provide the first complete account of catecholaminergic neurons in the zebrafish embryonic and juvenile brain. We identified four major th2-expressing neuronal groups that likely use dopamine as transmitter in the zebrafish diencephalon, including neurons of the posterior preoptic nucleus, the paraventricular organ, and the nuclei of the lateral and posterior recesses in the caudal hypothalamus. th2 Expression in the latter two groups resolves a previously reported discrepancy, in which strong dopamine but little tyrosine hydroxylase immunoreactivity had been detected in the caudal hypothalamus. Our data also confirm that there are no mesencephalic DA neurons in zebrafish. J. Comp. Neurol. 518:423–438, 2010. © 2009 Wiley-Liss, Inc.

Highlights

Expressing cells may use dopamine as a neurotransmitter, we included expression of dopamine beta hydroxylase, dopa decarboxylase, and dopamine transporter in our analysis
We identified four major th2expressing neuronal groups that likely use dopamine as transmitter in the zebrafish diencephalon, including neurons of the posterior preoptic nucleus, the paraventricular organ, and the nuclei of the lateral and posterior recesses in the caudal hypothalamus. th2 Expression in the latter two groups resolves a previously reported discrepancy, in which strong dopamine but little tyrosine hydroxylase immunoreactivity had been detected in the caudal hypothalamus
Catecholaminergic neurons modulate activity of other neurons in local as well as far-ranging circuits, and it is implicit that all CA groups be identified before studies of anatomy and function of circuits may be initiated

Summary

Introduction

Expressing cells may use dopamine as a neurotransmitter, we included expression of dopamine beta hydroxylase, dopa decarboxylase, and dopamine transporter in our analysis. We identified four major th2expressing neuronal groups that likely use dopamine as transmitter in the zebrafish diencephalon, including neurons of the posterior preoptic nucleus, the paraventricular organ, and the nuclei of the lateral and posterior recesses in the caudal hypothalamus. Dopamine (DA) and noradrenaline (NA) are the major catecholamines (CA) in the central nervous system (CNS; Bjorklund and Dunnett, 2007; Smeets and Gonzalez, 2000). The diencephalic DA groups correlate anatomically with A11, periventricular gray matter of thalamus, extending into midbrain; A12, tuberal cells of arcuate nucleus and adjacent periventricular nucleus; A13, zona incerta of ventral thalamus ( named prethalamus; Puelles and Rubenstein, 2003); A14, rostral periventricular group; and A15, preoptic area/rostral hypothalamus (Smeets and Gonzalez, 2000)

Methods

Results

Conclusion