Early development of the retina and pineal complex in the sea lamprey: Comparative immunocytochemical study

Abstract

Lampreys have a complex life cycle, with largely differentiated larval and adult periods. Despite the considerable interest of lampreys for understanding vertebrate evolution, knowledge of the early development of their eye and pineal complex is very scarce. Here, the early immunocytochemical organization of the pineal complex and retina of the sea lamprey was studied by use of antibodies against proliferating cell nuclear antigen (PCNA), opsin, serotonin, and gamma-aminobutyric acid (GABA). Cell differentiation in the retina, pineal organ, and habenula begins in prolarvae, as shown by the appearance of PCNA-negative cells, whereas differentiation of the parapineal vesicle was delayed until the larval period. In medium-sized to large larvae, PCNA-immunoreactive (-ir) cells were numerous in regions of the lateral retina near the differentiated part of the larval retina (central retina). A late-proliferating region was observed in the right habenula. Opsin immunoreactivity appears in the pineal vesicle of early prolarvae and 3 or 4 days later in the retina. In the parapineal organ, opsin immunoreactivity was observed only in large larvae. In the pineal organ, serotonin immunoreactivity was first observed in late prolarvae in photoreceptive (photoneuroendocrine) cells, whereas only a few of these cells appeared in the parapineal organ of large larvae. No serotonin immunoreactivity was observed in the larval retina. GABA immunoreactivity appeared earlier in the retina than in the pineal complex. No GABA-ir perikaryon was observed in the retina of larval lampreys, although a few GABA-ir centrifugal fibers innervate the inner retina in late prolarvae. First GABA-ir ganglion cells occur in the pineal organ of 15-17 mm larvae, and their number increases during the larval period. The only GABA-ir structures observed in the parapineal ganglion of larvae were afferent fibers, which appeared rather late in development. The time sequence of development in these photoreceptive structures is rather different from that observed in teleosts and other vertebrates. This suggests that the unusual development of the three photoreceptive organs in lampreys reflects specialization for their different functions during the larval and adult periods.

Light-induced degeneration and microglial response in the retina of an epibenthonic pigmented teleost: age-dependent photoreceptor susceptibility to cell death

“…There was a progressive thinning of the ONL in the constant light-treated larval tench retinas (Fig.2). CERN-922 polyclonal antibody has been found to be useful for labelling developing and mature photoreceptors in the retina of agnathans (Meléndez-Ferro et al, 2002;Villar-Cheda et al, 2008) and teleosts (Candal et al, 2005;Bejarano-Escobar et al, 2010), including the tench (Bejarano-Escobar et al, 2009). Immunoreactive photoreceptor cells were abundant in control retinas (Fig.3A), but light damage led to the progressive loss of labelled cells as the experimental treatment advanced (Fig.3B,C).…”

The ancestral role of nodal signalling in breaking L/R symmetry in the vertebrate forebrain

“…4a,b), providing evidence against conservation in the catshark of Fgf8 role in parapineal specification and migration. In the lamprey, the parapineal organ forms a second pineal outgrowth at the midline, rostrally to the pineal organ 18,30 , and projects to the left habenulae, although this occurs at larval stages 33 ( Supplementary Fig. 3).…”

The Spatial Relationship of γ-Aminobutyric Acid (GABA) Neurons and Gonadotropin-Releasing Hormone (GnRH) Neurons in Larval and Adult Sea Lamprey, <i>Petromyzon marinus</i>

“…In these studies, GABA, and agents that alter GABAergic function, significantly influenced reproductive processes by their actions on the hypothalamus and pituitary. A few studies have described GABA distribution in various parts of the agnathan nervous system, such as the retina [Rio et al, 1993[Rio et al, , 1996Meléndez -Ferro et al, 2002], spinal cord or brainstem motor systems [Batueva et al, 1990;Brodin et al, 1990;Meléndez -Ferro et al, 2000], and olfactory system [Meléndez-Ferro et al, 2001]. No studies have been done to indicate a role of GABA in regulating reproductive processes in lampreys.…”