Catecholaminergic systems in the zebrafish. II. Projection pathways and pattern of termination of the locus coeruleus

Abstract

The locus coeruleus is a widely projecting isthmal noradrenergic nucleus. In the zebrafish, it consists of between three and ten neurons, most of which have multiple, bilaterally projecting axons. Immunohodological studies show that the locus coeruleus provides most, if not all, of the noradrenergic innervation of the brain rostral to the isthmus. The pathways and targets in the zebrafish are similar to ascending coeruleal projections of other vertebrates. Axons ascend through two main pathways: the longitudinal catecholamine bundle and the periventricular catecholamine pathway. The former is a dense meshwork of varicosity-bearing axons which ascends along the lateral longitudinal fasciculus into the mesencephalon. In the posterior tuberal area, this bundle dives ventrally and assumes a lateral position. In the diencephalon, it takes up a position ventral to the medial forebrain bundle, and follows this bundle into the telencephalon, where it joins the medial olfactory tract to enter the olfactory bulb. The periventricular catecholamine pathway is a diffuse pathway consisting of thick, smooth axons. It is associated with the medial longitudinal fasciculus. Rostral to the nucleus of the medial longitudinal fasciculus, this pathway joins the longitudinal catecholamine bundle around the medial forebrain bundle. The periventricular pathway gives rise to coarse terminal arbors with large but sparse varicosities, whereas the longitudinal catecholamine bundle gives rise to terminal plexuses with fine and dense fibers and varicosities. Among the more densely innervated regions are the raphé nucleus, the interpeduncular nucleus, the torus semicircularis, parts of the hypothalamus, and the suprachiasmatic and preoptic areas. The torus longitudinalis, optic tectum, cerebellum, habenular complex, the dorsomedial zone of area dorsalis telencephali, and the olfactory bulb are moderately innervated. The nucleus glomerulosus, the torus lateralis and lateral subnuclei of the nucleus diffusus, and the anterior tuberal nucleus are devoid of noradrenergic innervation.

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

“…Furthermore, the amphibian TS, mammalian inferior colliculus (IC, TS homolog; Bass et al, 2005) and dorsal lateral mesencephalic nucleus in birds (MLd, IC homolog; Karten, 1967) all receive substantial CAergic input (Appeltants et al, 2001;Endepols et al, 2000;Kitahama et al, 1996;Klepper and Herbert, 1991;Mello et al, 1998;Tong et al, 2005), which suggests a conserved pattern and modulatory role of CAs on central auditory processing across vertebrates. The primary source of NAergic fibers is likely the LC (Ma, 1994) as is the case in mammals (Hormigo et al, 2012;Klepper and Herbert, 1991) and birds (Kitt and Brauth, 1986a) since projection patterns of NAergic neurons are highly conserved (Smeets and Gonzalez, 2000;Tay et al, 2011). Furthermore, small clusters of retrogradely filled cells are found in the isthmus just dorsomedial to the lateral lemniscus after neurobiotin injection into the TSnc in midshipman .…”

“…This robust pattern of TH-ir in TS appears to be consistent across teleosts and is likely a mixture of DA and NAergic input, as there are reports of DBH, TH, and DA-ir fibers and terminals in this area across a variety of species (e.g., Adrio et al, 2002;Batten et al, 1993;Corio et al, 1991;Ekstrom et al, 1990;Ekstrom et al, 1986;Hornby and Piekut, 1990;Kaslin and Panula, 2001;Ma, 1994;Roberts et al, 1989;Sas et al, 1990;Vetillard et al, 2002). Furthermore, the amphibian TS, mammalian inferior colliculus (IC, TS homolog; Bass et al, 2005) and dorsal lateral mesencephalic nucleus in birds (MLd, IC homolog; Karten, 1967) all receive substantial CAergic input (Appeltants et al, 2001;Endepols et al, 2000;Kitahama et al, 1996;Klepper and Herbert, 1991;Mello et al, 1998;Tong et al, 2005), which suggests a conserved pattern and modulatory role of CAs on central auditory processing across vertebrates.…”

“…In addition, neurobiotin injections into PAG indicate projections from this area as well (Kittelberger and Bass, 2013). In general, projections from LC are thought to be highly conserved and provide the majority of NAergic fibers in the midbrain and forebrain (Ma, 1994;Tay et al, 2011). In songbirds, LC projects widely to forebrain song circuitry (Appeltants et al, 2001;2002a;Castelino et al, 2007), but less is known of its direct projections to less derived vocal areas (Castelino and Schmidt, 2010).…”

Noradrenergic neurons in the zebrafish hindbrain are induced by retinoic acid and requiretfap2afor expression of the neurotransmitter phenotype

“…Two main groups of noradrenergic (NA) neurons, a caudal rhombencephalic group (A1-A3, in medulla and area postrema) and a rostral rhombencephalic group (A4-A7, in the locus coeruleus), can be recognized in the hindbrain of higher vertebrates (Smeets and Reiner, 1994;Smeets and Gonzalez, 2000) as well as in zebrafish (Ma, 1994a;Ma, 1994b;Ma, 1997;Holzschuh et al, 2001). The control of noradrenergic development in the mouse hindbrain has mainly been studied in the locus coeruleus (reviewed by Goridis and Rohrer, 2002), where important roles have been demonstrated for Mash1 (Hirsch et al, 1998), Phox2a (Morin et al, 1997), Phox2b (Pattyn et al, 1999) and Tlx3 (Qian et al, 2001).…”

Evolution and expression of D2 and D3 dopamine receptor genes in zebrafish

“…Several reports have now described the organization and function of the dopamine system in zebrafish. Clusters of dopaminergic neurons have been identified in the developing embryo (Guo et al, 1999;Holzschuh et al, 2001;Rink and Wullimann, 2002b) and adult (Ma, 1994a(Ma, , b, 1997(Ma, , 2003. Immunocytochemical evidence suggests that zebrafish have a conserved dopaminergic projection pathway that is homologous to the human mesostriatal pathway (Rink and Wullimann, 2002a).…”