Organization of the Serotonergic System in the Central Nervous System of Two Basal Actinopterygian Fishes: the Cladistians <b><i>Polypterus senegalus</i></b> and <b><i>Erpetoichthys calabaricus</i></b>

Abstract

Cladistians (Polypteriformes) are currently considered basal to other living ray-finned fishes (actinopterygians), and their brain organization is therefore critical to providing information about the primitive neural characters that existed in the earliest ray-finned fishes. The organization of the serotonergic system in the brain has been carefully analyzed in most vertebrate groups, and in the present study we provide the first detailed information on the distribution of serotonergic cell bodies and fibers in the central nervous system of representative species of the two extant genera of cladistians, i.e. Polypterus senegalus and Erpetoichthys calabaricus, by means of immunohistochemistry against serotonin (5-HT). Distinct groups of immunoreactive cells were detected in the preoptic area, the hypothalamic paraventricular organ, the pineal organ, the pretectal region, the long column of the raphe in the rhombencephalic midline, the spinal cord, and amacrine cells in the inner nuclear layer of the retina. Fiber labeling was widely distributed in all main brain subdivisions but was more abundant in distinct pallial and subpallial areas, the preoptic area, the thalamus, the optic tectum, the tori semicircularis and lateralis, the rhombencephalic reticular formation, the nucleus of the solitary tract, and the dorsal aspect of the spinal cord. Our analysis makes it possible to establish which serotonergic structures characterized the earliest ray-finned fishes, and a comparison of these results with those from other classes of vertebrates, including a segmental analysis to correlate cell populations, reveals that most characteristics, such as the presence of serotonergic cells in the preoptic area and the basal hypothalamus, are preserved in all anamniotes. However, this system seems to be reduced in amniotes, mainly mammals, although important features are shared, such as the presence of serotonergic cells in the pineal organ, the retina, and the raphe nuclei.

Serotonin‐immunoreactivity in the brain of the cichlid fish Oreochromis mossambicus

“…In addition, Rodríguez-G omez et al (2000) reported 5-HT-ir axons near the lateral forebrain bundles in the Senegalese sole, whereas in this study, we observed 5-HT-ir fibers in the lateral forebrain bundle in the tilapia. Furthermore, the absence of 5-HT-ir cells in the telencephalon of the tilapia is consistent with other groups such as agnathans, elasmobranchs, cladistians, holosteans, teleosts, and sarcopterygians (Abalo et al, 2007;Chiba & Oka, 1999;Ekström & Van Veen, 1984;Kah & Chambolle, 1983;L opez & Gonz alez, 2014L opez & Gonz alez, , 2015Lozano et al, 2020;Meek & Joosten, 1989;Parent & Northcutt, 1982;Reiner & Northcutt, 1992;Rodríguez-G omez et al, 2000;Stuesse et al, 1990;Yamanaka et al, 1990) except for their presence in evolutionarily ancient sturgeons (Adrio et al, 1999) and in a viviparous teleost G. affinis (Bhat & Ganesh, 2021).…”

“…Especially, the diversity of phylogenetically ancient vertebrates like fish is greater than that of any other taxon. Among fishes, the occurrence of 5-HT has been studied in the brain of agnathans (Kadota, 1991;Pierre et al, 1992;Steinbusch & Nieuwenhuys, 1979), chondrichthyes (Carrera et al, 2008;Stuesse et al, 1990Yamanaka et al, 1990), and in actinopterygians that include cladistians (polypteriformes), chondrosteans (Acipenseriformes), holosteans (Amiiformes and Lepisosteiformes), and teleosts (Adrio et al, 1999;Chiba & Oka, 1999;L opez & Gonz alez, 2014;Lozano et al, 2020;Parent & Northcutt, 1982;Prasad et al, 2015;Reiner & Northcutt, 1992). The distribution pattern of 5-HT-ir neurons has been reported in different groups of teleosts, for example, in the goldfish Carassius auratus (Kah & Chambolle, 1983), the catfish Clarias gariepinus (Corio et al, 1991), the Senegalese sole Solea senegalensis (Rodríguez-G omez et al, 2000), the zebrafish (Kaslin & Panula, 2001), the grunting toadfish Allenbatrachus grunniens, the Columbian shark catfish Ariopsis seemanni, the upside-down catfish Synodontis nigriventris (Rosner et al, 2020), the plainfin midshipman Porichthys notatus (Timothy & Forlano, 2020), and in the mosquitofish Gambusia affinis (Bhat & Ganesh, 2021).…”

Distribution of the transcription factor islet‐1 in the central nervous system of nonteleost actinopterygian fish: Relationship with cholinergic and catecholaminergic systems

“…The nomenclature used is essentially the same followed in previous studies of the brain in nonteleost actinopterygian fishes (González et al., 2014; Jiménez et al., 2020; López & González, 2014; López et al., 2013, 2014, 2016, 2017, 2019, 2022; Lozano et al., 2018, 2019, 2020; Morona et al., 2013).…”

“…Regarding the mesencephalon, few studies consider the presence of the mesencephalic nucleus of the trigeminal nerve, and fewer discuss the possible Isl1 immunoreactivity of its cells, although it has been demonstrated in chicken and mouse (Hunter et al, 2001;Lipovsek et al, 2017;Sun et al, 2008), proving the expression of the transcription factor during the development of these cells in gnathostomes and its further maintenance.…”

Predicting the Distribution of Serotonergic Axons: A Supercomputing Simulation of Reflected Fractional Brownian Motion in a 3D-Mouse Brain Model

“…The self-organization of the brain serotonergic matrix remains an unsolved problem in neuroscience. This matrix, or a meshwork of axons (fibers), is present in virtually all brain regions, likely across the entire vertebrate clade (Wolters et al, 1985; Stuesse et al, 1991; Metzger et al, 2002; López and González, 2014; Janušonis, 2018; Awasthi et al, 2020). It appears to be fundamentally associated with neuroplasticity (Lesch and Waider, 2012; Daws et al, 2022), raising new questions (Vargas et al, 2023), and is remarkable in its ability to robustly regenerate in the adult mammalian brain (Jin et al, 2016; Cooke et al, 2022).…”