Neuronal organization of the melanin‐concentrating hormone system in primitive actinopterygians: Evolutionary changes leading to teleosts

Abstract

Hypothalamic melanin-concentrating hormone (MCH) neurones occur in all vertebrates and have an apparent neuromodulatory role. In teleost fish, however, MCH is used also as a neurohypophysial hormone, controlling skin color, and as a hypophysiotrophic peptide. This work describes the central location of immunoreactive MCH perikarya and their projections to the pituitary in a range of ancestral fish to determine the phylogenetic stage when the peptide adopted these roles. In all actinopterygians examined, including polypteriformes, chondrosteans, holosteans, and teleosts, immunoreactive fibers were abundant in the median eminence or, in the case of teleosts, within the pars distalis itself, suggesting MCH acquired a hypophysial regulatory role early in vertebrate evolution. MCH fibers appeared to be absent from the posterior neurohypophysis of the polypteriform Calamoichthys but were evident in this region in the chondrostean Acipensor, the holosteans Lepisosteus and Amia, and all teleosts, suggesting its use as a neurohypophysial hormone. The ability of MCH to induce skin pallor seems to have arisen at a later stage, probably in the preholosteans. This hormonal role coincides with the migration of MCH perikarya away from the ventricular surface and their enlargement into magnocellular neurones. In the higher teleosts, magnocellular hypothalamo-neurohypophysial neurones predominate in size and number, whereas smaller periventricular MCH neurones associated with the paraventricular organ, that are prominent in lampreys, early actinopterygians and tetrapods, are reduced in teleosts. The data suggest that, in teleost fish, earlier functions of the peptide may have become subordinate to its novel pigmentary role.

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

“…Similar MCH-mRNA-expressing cell clusters have been previously reported in several teleost species including rainbow trout [35], cichlid fish, Cichlasoma dimerus [7], tilapia [4], barfin flounder [6] gilthead seabream [5] and eel [36]. 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].…”

“…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. Similar MCH-mRNA-expressing cell clusters have been previously reported in several teleost species including rainbow trout [35], cichlid fish, Cichlasoma dimerus [7], tilapia [4], barfin flounder [6] gilthead seabream [5] and eel [36]. 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].…”

“…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. In teleosts, the majority of MCH neurons migrate from the periventricular areas and it is within euteleosts that hypothalamic-hypophyseal neurons of the lateral part of the lateral tuberal nucleus represent the most prominent MCH-producing area [36]. The number and size of MCH cell bodies associated with the PVO is highly variable [36], and in the goldfish there are two relatively prominent neuronal groups in this area, similar to the rainbow trout [35] and eel [36].…”

“…In teleosts, the majority of MCH neurons migrate from the periventricular areas and it is within euteleosts that hypothalamic-hypophyseal neurons of the lateral part of the lateral tuberal nucleus represent the most prominent MCH-producing area [36]. The number and size of MCH cell bodies associated with the PVO is highly variable [36], and in the goldfish there are two relatively prominent neuronal groups in this area, similar to the rainbow trout [35] and eel [36]. The function of these caudal hypothalamic MCH neurons is unknown, but a specific increase in MCH-mRNA levels has been observed in repeatedly disturbed tilapia [9].…”

Multifunctional Roles of Melanocyte-Stimulating Hormone and Melanin-Concentrating Hormone in Fish: Evolution from Classical Body Color Change

“…In mammals, mchr1 transcripts are distributed wider than mchr2 transcript (Boutin et al 2002;Schlumberger et al 2002;Eberle et al 2004). The wide distribution of mchr2 transcripts in peripherals coincides with the role of MCH as a neurohypophysial hormone as shown by extensive projections of the neuron from the hypothalamus to PN in ray-finned fish including barfin flounder (Naito et al 1985;Batten and Baker 1988;Minth et al 1989;Mancera and Fernández-Llebrez 1995;Baker and Bird 2002;Amano et al 2003).…”