Differential distribution of hypocretin (orexin) and melanin‐concentrating hormone in the goldfish brain

Abstract

The orexigenic peptides hypocretin (orexin) and melanin-concentrating hormone (MCH) are involved in the control of food intake and in other homeostatic functions including sleep and arousal. In this article we study the distribution of these peptides in the brain of the goldfish (Carassius auratus), focusing on those regions particularly related to feeding, sleep, and arousal. Although the general distribution of these peptides in goldfish shows many similarities to those described previously in other species, we observed some noteworthy differences. As in other vertebrates, the peptidergic somata lie in the anterolateral hypothalamus. In goldfish, both hypocretin and MCH immunoreactive cell bodies project fibers to the ventral telencephalon, thalamus, and hypothalamus. At mesencephalic levels fibers reach the deep layers of the optic tectum and also course sparsely through the mesencephalic tegmentum. In contrast to the strong innervation of locus coeruleus and raphe in mammal, the MCH and hypocretin systems in goldfish barely innervate these aminergic populations related to the regulation of sleep and arousal. MCH, but not hypocretin, immunoreactive fibers terminate substantially in the sensory layer of the vagal gustatory lobe of goldfish, while both peptidergic systems distribute to the primary visceral sensory areas of the medulla and pons. The strong involvement of these peptidergic systems with the hypothalamus and general visceral nuclei, but not with locus coeruleus or raphe nuclei support the view that these peptides originally played a role in regulation of energy balance and evolved secondarily to influence sleep-wakefulness systems in amniote vertebrates.

Distribution of Orexin/Hypocretin Immunoreactivity in the Brain of the Lungfishes <i>Protopterus dolloi</i> and <i>Neoceratodus forsteri</i>

“…This result is in line with similar observations from several studies in teleosts, amphibians, reptiles, birds, and mammals [Shibahara et al, 1999;Galas et al, 2001;Phillips-Singh et al, 2003;Kaslin et al, 2004;Huesa et al, 2005;Singletary et al, 2005Singletary et al, , 2006Nixon and Smale, 2007;. In contrast, orexins in specific cells of the adenohypophysis have been reported in human [Blanco et al, 2003], orexin-A in two species of anurans [Yamamoto et al, 2004;Suzuki et al, 2007], and orexin-A and orexin-B in the pituitary of two species of teleost fishes [Amiya et al, 2007;Suzuki et al, 2007Suzuki et al, , 2009.…”

“…In zebrafish (Danio rerio) , orexin-ir cells are segregated into two populations, one along the third ventricle within the preoptic area and suprachiasmatic nucleus and the other within the anterior hypothalamus [Kaslin et al, 2004;Faraco et al, 2006]. The presence of these cells in the goldfish (Carassius auratus) brain is more restricted and they are located in the anterolateral hypothalamus within the nucleus lateralis tuberis and, more caudally, bordering the third ventricle in the nucleus posterioris periventricularis [Huesa et al, 2005]. The latter nucleus contains the main group of orexin-ir cells in the medaka fish Oryzias latipes [Amiya et al, 2007].…”

“…Interestingly, the primary amino acid sequence of orexins is highly conserved across vertebrates [Sakurai et al, 1998;Shibahara et al, 1999;Alvarez and Sutcliffe, 2002;Ohkubo et al, 2002;Panula, 2009]. Thus, the distribution of orexin-like immunoreactive cells and fibers in the brain of different vertebrates has been analyzed by means of immunohistochemical techniques using antibodies against mammalian orexins [Shibahara et al, 1999;Galas et al, 2001;Ohkubo et al, 2002;PhillipsSingh et al, 2003;Kaslin et al, 2004;Huesa et al, 2005;Singletary et al, 2005Singletary et al, , 2006Amiya et al, 2007;. In general, the localization of orexin-ir cell bodies in particular forebrain nuclei and the widespread distribution of fibers were corroborated for all vertebrate groups studied, but when direct cross-species comparisons were made, using the same immunohistochemical approach, important variations were found in the precise distribution of orexin-ir cells and fibers [Singletary et al, 2006;Nixon and Smale, 2007;.…”

Regulation of the Hypothalamic Melanin-Concentrating Hormone Neurons by Sex Steroids in the Goldfish: Possible Role in the Modulation of Luteinizing Hormone Secretion

“…The dorsal population seems to be associated with the paraventricular organ (PVO), within the so-called dorsal area of the lateral recess nucleus, whereas the ventral MCH-expressing population is placed within the ventral part of the lateral recess nucleus. Immunohistochemical studies in the goldfish have also reported the presence of MCH-immunoreactive cell bodies within the lateral part of the lateral tuberal nucleus [34]. However, the latter study did not describe the presence of MCH-producing cells associated to the PVO within the caudal hypothalamus but immunoreactive cell bodies were reported within the zona limitans.…”

“…Hypothalamic-hypophyseal neurons in the lateral tuberal nucleus respond strikingly to background color changes and constitute the most prominent MCH-mRNA-expressing cell cluster in the teleost brain [36]. Most of the axons of the MCH-producing cells from the lateral tuberal nucleus project to the pituitary [37] but studies in several species including goldfish have further reported dense MCH innervation within all main brain regions [34]. Evolutionary studies on the organization of MCH perikarya within the hypothalamus have reported that a MCH-producing cell cluster within the lateral tuberal nucleus is first seen in the holostean species, tentatively coinciding with the newly acquired pigmentary role of MCH.…”