Comparative Distribution of 2[¹²⁵I]Iodomelatonin Binding in the Brains of Diurnal Birds: Outgroup Analysis with Turtles

Abstract

The roles that the pineal gland and its hormone melatonin play in the regulation of circadian rhythmicity and photoperiodism vary among vertebrate species. Recently, putative sites of melatonin action have been elucidated in several avian and mammalian species by application of in vitro binding of a radioiodinated melatonin agonist, 2[¹²⁵I]iodomeIatonin (IMEL) and autoradioradiography. These studies in mammals, birds and reptiles have indicated profound differences in the distribution of IMEL binding between these diverse groups, suggesting that these large differences in binding may reflect differences in melatonin function. The present study was performed to determine systematically whether the variance in IMEL binding among avian species corresponds to changes in circadian organization and/or phylogenetic relationships. The distribution of specific IMEL binding was determined in the brains from birds belonging to 14 different species in 5 Orders (Psittaciformes, Passeriformes, Columbiformes, Galliformes and Anseriformes) using in vitro binding, autoradiography and computer-assisted image analysis. The distribution was compared to a similar study in 3 species of turtles as an outgroup. The data indicated IMEL binding in retinorecipient structures of the circadian, tectofugal, thalamofugal and accessory optic visual pathways in all avian species. Relay nuclei and integrative structures of the tectofugal, thalamofugal, accessory optic, and limbic systems, however, bound the hormone to varying degrees. In turtles, binding was observed in retinorecipient structures of the thalamofugal visual pathway and in retinorecipient and integrative areas of the tectofugal visual pathway. No binding was observed in the pineal gland, tuberal hypothalamus or adenohypophysis in any avian or testudine species. This distribution is drastically different from that observed in mammals, where binding predominates in the pars tuberalis of the adenohypophysis and in the suprachiasmatic nucleus, suggesting that the circadian system may influence a wide array of sensory and integrative functions in birds and reptiles through the circadian secretion of melatonin, but that this capacity has been lost in mammals.

Melatonin Receptors in the Pituitary of a Teleost Fish: mRNA Expression, 2-[¹²⁵I]Iodomelatonin Binding and Cyclic AMP Response

“…This binding was weak in comparison to the binding observed on tissue sections from the brain, such as those passing through the optic tectum. Our results contrast with previous investigations indicating that no melatonin binding sites are present in the pituitary of nonmammalian vertebrates including birds [19]and fish [33, 35, 36]. Also, melatonin receptor gene expression was not detected in the trout [36].…”

“…Part of the circadian effects of melatonin are mediated through its action on the hypothalamic circadian clocks (the suprachiasmatic nuclei, SCN) in mammals, and the visual (v)SCN in birds [5, 7, 16, 17, 18, 19, 20, 21, 22]. The reproductive effects of melatonin have been clearly demonstrated in mammals [23, 24], and the targets include the premammillary and mediobasal areas of the hypothalamus (to modulate LH secretion) and the pars tuberalis of the adeno-hypophysis (involved in the seasonal control of prolactin secretion) [24, 25, 26].…”

“…To date, the available data differ with gender, photoperiod and temperature administration, and reproductive stage, so that no clear-cut picture arises. This is further complicated by the observation that the 125 I-melatonin binding sites display a widespread distribution in nonmammals [19, 29, 30, 31, 32, 33]. The first, and to date the only, direct indication that melatonin might be involved in the photoperiodic control of reproduction came from a study in the Atlantic croaker fish reporting that (1) intraventricular melatonin administration increased plasma gonadotropin hormone (GtH II), and (2) physiological concentrations of melatonin stimulated GtH II release from cultured pituitary fragments [34].…”

“…The first, and to date the only, direct indication that melatonin might be involved in the photoperiodic control of reproduction came from a study in the Atlantic croaker fish reporting that (1) intraventricular melatonin administration increased plasma gonadotropin hormone (GtH II), and (2) physiological concentrations of melatonin stimulated GtH II release from cultured pituitary fragments [34]. This is in marked contrast with the results reporting no binding of melatonin in the pituitary of the fish and birds investigated thus far by autoradiography binding [19, 33, 35, 36]; although, Iigo et al [37]suggested – but on the basis of one single point measurement only – that binding sites might be present. In addition, the partial cloning of three melatonin receptor subtypes in the trout did not allow detection of an expression in the pituitary by in situ hybridization [36].…”

Differential Expression of Melatonin Receptor Subtypes MelIa, MelIb and MelIc in Relation to Melatonin Binding in the Male Songbird Brain

“…Because the general pattern of IMEL binding in the avian brain has been reported in detail in previous studies, including various songbird species [Dubocovich et al, 1989;Cozzi et al, 1993;Cassone et al, 1995;Gahr and Kosar, 1996;Whitfield-Rucker and Cassone, 1996;Bentley and Ball, 2000;Aste et al, 2001], we focus here on the differential expression of the three MelR subtypes in the same brain regions and compare IMEL binding with MelR expression. In particular, we focus on areas which are either known to be melatonin sensitive or are being intensively investigated as part of a model system, or have strong IMEL binding and/or MelR expression.…”