Early development and organization of the retinopetal system in the larval sea lamprey, Petromyzon marinus L.

Rodicio, Marı́a Celina; Pombal, Manuel A.; Anadón, Ramón

doi:10.1007/bf00187182

Cited by 31 publications

(27 citation statements)

References 40 publications

(46 reference statements)

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“…For example, previous tract-tracing studies of the oculomotor and retinopetal nuclei of the sea lamprey have shown that the number of retrogradely labeled neurons in these systems increases markedly throughout the larval period (Pombal et al, 1994;Rodicio et al, 1995), which is consistent with the continued presence of PCNA-ir cells in ventricular regions adjacent to these nuclei (present results). However, for most brain regions there are no data on the growth of neuronal populations.…”

Section: Late-proliferating Regionssupporting

confidence: 88%

Cell proliferation in the forebrain and midbrain of the sea lamprey

Villar-Cheda

Pérez-Costas

Meléndez-Ferro

et al. 2005

J of Comparative Neurology

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Cell proliferation in the forebrain and midbrain of the sea lamprey (Petromyzon marinus L.) was investigated by proliferation cell nuclear antigen (PCNA) immunocytochemistry, with BrdU labeling as a complementary technique. Correspondence between proliferation regions and areas of early neuronal differentiation was also assessed using antibodies against HNK-1 early differentiation marker. The brain of late embryos shows a homogeneously thick ventricular zone (VZ) containing PCNA-immunoreactive (PCNA-ir) nuclei. In early prolarvae, several discontinuities formed by PCNA-negative cells, and differences among regions in VZ thickness, become apparent. In late prolarvae and early larvae, these differences in VZ thickness and appearance, as well as the presence of PCNA-negative discontinuities, allowed us to correlate proliferation domains and neuroanatomical regions. In larvae, the number of PCNA-ir cells in the VZs diminish gradually, although a few PCNA-ir cells are present in the ependyma of most regions. In late larvae, proliferation becomes confined to a few ventricular areas (medial pallium, caudal habenula, ventral preoptic recess near the optic nerve, and tuberal portion of the posterior hypothalamic recess). During metamorphosis there appears to be no proliferation, but in upstream adults a few PCNA-ir cells are observed in the most caudal habenula. The characteristics of the proliferative regions revealed in lamprey with PCNA immunocytochemistry show notable differences from those observed in other vertebrates, and these differences may be related to the peculiar life cycle of lampreys.

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Section: Late-proliferating Regionssupporting

confidence: 88%

Cell proliferation in the forebrain and midbrain of the sea lamprey

Villar-Cheda

Pérez-Costas

Meléndez-Ferro

et al. 2005

J of Comparative Neurology

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“…Following application of biocytin in the eye bulb, both retinofugal and retinopetal connections were revealed, as previously reported by using other techniques [Kennedy and Rubinson, 1977;Kosareva, 1980;Repérant et al, 1980Repérant et al, , 1982Vesselkin et al, 1980Vesselkin et al, , 1984Vesselkin et al, , 1996Vesselkin and Repérant, 1985;De Miguel et al, 1990;Rodicio et al, 1995]. Briefly, retinofugal fibers of the optic tract projected mostly to the superficial layers of the contralateral OT (SM and SO) and constituted the lateral and axial optic tracts, whereas the retinopetal cells distributed in the M5 nucleus of Schöber and the mesencephalic reticular area ( fig.…”

Section: Complementary Experimentssupporting

confidence: 49%

“…Some large dorsal dendrites coursed in the OT, where some cell bodies could also be observed. The M5 nucleus of Schöber and the mesencephalic reticular area are two well-known retinopetal nuclei in lampreys [Kosareva, 1980;Repérant et al, 1980Repérant et al, , 1982Vesselkin et al, 1980Vesselkin et al, , 1984Vesselkin et al, , 1996Vesselkin and Repérant, 1985;Rodicio et al, 1995]. These studies showed that the retinopetal cells send their axons rostrally through the axial optic tract on the way to the retina and have long dendrites that can reach the OT.…”

Section: Afferent Connections Of the Adult Lamprey Otmentioning

confidence: 97%

“…Unilateral injections in the OT led to labeling of cells inside the limits of the ipsilateral and contralateral retinopetal nuclei. Those located periventricularly correspond to the M5 nucleus of Schöber, whereas those located laterally that can reach the ventrolateral OT belong to the mesencephalic reticular area [see Rodicio et al, 1995;Vesselkin et al, 1996]. Some of the mesencephalic retinopetal cells have long dorsal dendrites that reach the OT [Vesselkin et al, 1984[Vesselkin et al, , 1996De Miguel et al, 1990;Río et al, 1993].…”

Section: Mesencephalic Projectionsmentioning

confidence: 99%

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Afferent Connections of the Optic Tectum in Lampreys: An Experimental Study

Arriba

Pombal²

2006

Brain Behav Evol

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Tectal afferents were studied in adult lampreys of three species (Ichthyomyzon unicuspis, Lampetra fluviatilis, and Petromyzon marinus) following unilateral BDA injections into the optic tectum (OT). In the secondary prosencephalon, neurons projecting to the OT were observed in the pallium, the subhipoccampal lobe, the striatum, the preoptic area and the hypothalamus. Following tectal injections, backfilled diencephalic cells were found bilaterally in: prethalamic eminence, ventral geniculate nucleus, periventricular prethalamic nucleus, periventricular pretectal nucleus, precommissural nucleus, magnocellular and parvocellular nuclei of the posterior commissure and pretectal nucleus; and ipsilaterally in: nucleus of Bellonci, periventricular thalamic nucleus, nucleus of the tuberculum posterior, and the subpretectal tegmentum, as well as in the pineal organ. At midbrain levels, retrogradely labeled cells were seen in the ipsilateral torus semicircularis, the contralateral OT, and bilaterally in the mesencephalic reticular formation and inside the limits of the retinopetal nuclei. In the hindbrain, tectal projecting cells were also bilaterally labeled in the dorsal and lateral isthmic nuclei, the octavolateral area, the sensory nucleus of the descending trigeminal tract, the dorsal column nucleus and the reticular formation. The rostral spinal cord also exhibited a few labeled cells. These results demonstrate a complex pattern of connections in the lamprey OT, most of which have been reported in other vertebrates. Hence, the lamprey OT receives a large number of nonvisual afferents from all major brain areas, and so is involved in information processing from different somatic sensory modalities.

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“…Previous studies with tract-tracing methods for the sea lamprey have suggested that this system appears later than was in fact observed here, given the absence or rarity of labeled M5 neurons after horseradish peroxidase application to the eye in larvae between 11 and 20 mm in length (Rodicio et al, 1995). The present immunocytochemical results revealed the presence of GABAergic centrifugal fibers in prolarval eyes, which is earlier than previously thought and only a few days latter than the start of differentiation of the first photoreceptors.…”

Section: Development Of Gabaergic Structures In the Retina And Pinealcontrasting

confidence: 46%

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

Meléndez-Ferro

Villar-Cheda

Abalo

et al. 2001

J of Comparative Neurology

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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.

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Early development and organization of the retinopetal system in the larval sea lamprey, Petromyzon marinus L.

Cited by 31 publications

References 40 publications

Cell proliferation in the forebrain and midbrain of the sea lamprey

Cell proliferation in the forebrain and midbrain of the sea lamprey

Afferent Connections of the Optic Tectum in Lampreys: An Experimental Study

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

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