Extensive presence of serotonergic cells and fibers in the peripheral nervous system of lampreys

Abstract

Lampreys are suitable animal models for studying the evolution of the vertebrate nervous system because they belong to the earliest group of extant vertebrates, the agnathans. The general organization of the serotonergic central nervous system is well known in lampreys, but information about its peripheral organization is lacking. In the present study, high-performance liquid chromatography and immunohistochemistry with an antibody against serotonin were used to study the presence and peripheral distribution of serotonergic elements in the head of larval sea lampreys. Adult lampreys were also analyzed in order to compare the organization of the system in larval and postmetamorphic stages. Serotonergic cells were observed in the cranial nerve ganglia, the musculature, the taste buds, and in the gills. Serotonergic fibers were extensive in all tissues except the epidermis. Possible roles were proposed for the different cell types observed in relation to their location, structure, and innervation patterns. The serotonergic cells appear to be involved in the oxygen and taste chemoreception processes, the modulation of musculature contraction, and in the regulation of cilia beat frequency and mucus secretion in lampreys. The extensive presence of serotonergic elements in the peripheral nervous system of lampreys suggests a close relationship with the organization of this system in invertebrate groups.

Evolution of the hypoxia-sensitive cells involved in amniote respiratory reflexes

“…Serotonergic cells in lamprey gills are proposed to correspond to the gill NECs of jawed fishes (Barreiro-Iglesias et al, 2009). We detected putative NECs from embryonic day (E)18.5, in clusters on the medial edges of the gills, intimately associated with HNK1 epitope-immunoreactive neurites (Figure 4d).…”

“…DiI-labeled neural crest cells migrated into the branchial arches and contributed to the branchial arch basket, as expected (McCauley and Bronner-Fraser, 2003), but putative NECs in the gills and orobranchial epithelia, despite being near DiI-labeled cells, were unlabeled (n = 19; Figure 4i,j,n; Figure 4—figure supplement 1).

10.7554/eLife.21231.010Figure 4.Putative lamprey NECs are not neural crest-derived.( a ) Schematic larval lamprey section (modified from Barreiro-Iglesias et al, 2009) showing gill pairs in the orobranchial cavity, supported by an interbranchial septum, and a single gill at higher power. ( b ) Schematic Piavis-stage 17 (E19) lamprey (modified from Tahara,1988).

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“…( a ) Schematic larval lamprey section (modified from Barreiro-Iglesias et al, 2009) showing gill pairs in the orobranchial cavity, supported by an interbranchial septum, and a single gill at higher power. ( b ) Schematic Piavis-stage 17 (E19) lamprey (modified from Tahara,1988).…”

The Gustatory System of Lampreys

“…However, the location of the taste buds of adult lampreys in the water (respiratory) tube and not in a common respiratory and digestive tract as in larvae suggests that pharyngeal buds of lampreys may serve other purposes, e.g. possible evaluation of oxygen levels in respiratory water [Baatrup, 1983b], as recently suggested for other serotonergic peripheral cell types in gills of lampreys [Barreiro-Iglesias et al, 2009]. In any case, the location of the taste buds in the respiratory water tube does not exclude the possibility that they play a role in the detection of taste substances that are dissolved in the surrounding water.…”

Xenopus embryonic epidermis as a mucociliary cellular ecosystem to assess the effect of sex hormones in a non-reproductive context

“…Xenacoelomorpha species also display MCE features, such as the larval and adult epidermis of Xenoturbella (Xenoturbellida), which is composed of MS cells and MC cells with abundant mitochondria and microvilli [17], and the planarian (Platyhelminthes, Turbellaria) epidermis composed of MC-MS cells and ion-sensitive cells [18,19]. Multiple biological functions can be carried out by mucociliary epithelia, including the production of currents for food ingestion [3,5] or gamete transport [15,16], animal displacement [18], protection from exogenous noxious substances by mucus clearance [3,13,14] or mucus trapping [13], and ionic balance in response to serotonin [5] or gases [5,19]. MCE features are also generated in non-physiological contexts, such as induced ciliogenesis via androgen/anti-estrogen stimulation in mammalian female prostate (skene glands) [20], and the bronchogenic/foregut cysts processes in liver, renal pelvis and other organs [21,22].…”