Skip to main content
SpringerLink
Log in

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

An HRP study

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Development of the retinopetal system of the larval sea lamprey, Petromyzon marinus, was investigated following labelling of this system by injection of horseradish peroxidase into the orbit. This study extends our previous report on larval stages and provides a detailed description of the development of this system. We present quantitative and qualitative evidence suggesting that the retinopetal nuclei of Schober's M2-M5 nucleus, the mesencephalic reticular area and the tectum arise sequentially in that order, that the three retinopetal nuclei originate from a common anlage in the ventricular zone of the mesencephalic tegmentum and that the retinopetal cell population increases throughout the larval period. No neuronal death was observed. We also describe and discuss the significance of a transitory phase of retinopetal cell differentiation characterized by the presence of ventricular dendrites. Finally, we compare the development of retinopetal and retinofugal systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anadón R, De Miguel E, González MJ, Rodicio MC (1989) HRP study of the central components of the trigeminal nerve in the larval sea lamprey: organization and homology of the primary medullary and spinal nucleus of the trigeminus. J Comp Neurol 283:602–610

    Google Scholar 

  • Bourrat F, Sotelo C (1986) Neuronal migration and dendritic maturation of the medial cerebellar nucleus in rat embryos: an HRP in vitro study using cerebellar slabs. Brain Res 378:6985

    Google Scholar 

  • Cajal SR (1889) Sur la morphologie et les connexions des éléments de la retine des oiseaux. Anat Anz 4:111–121

    Google Scholar 

  • Cajal SR (1909) Histologie du système nerveux de l'homme et des vertébrés. Maloine, Paris (reprinted by CSIC, Madrid 1955)

    Google Scholar 

  • Clarke PGH (1982) The generation and migration of the chick's isthmic complex. J Comp Neurol 207:208–222

    Google Scholar 

  • Clarke PGH (1992) Neuron death in the developing avian isthmo-optic nucleus, and its relation to the establishment of functional circuitry. J Neurobiol 23:1140–1158

    Google Scholar 

  • Clarke PGH, Cowan WM (1976) The development of the isthmo-optic tract in the chick, with special reference to the occurrence and correction of developmental errors in the location and connections of isthmo-optic neurons. J Comp Neurol 167:143–164

    Google Scholar 

  • Clarke PGH, Rogers LA, Cowan WM (1976) The time of origin and the pattern of survival of neurons in the isthmo-optic nucleus of the chick. J Comp Neurol 167:125–142

    Google Scholar 

  • Crapon de Caprona M-D, Fritzsch B (1983) The development of the retinopetal nucleus olfactoretinalis of two cichlid fish as revealed by horseradish peroxidase. Dev Brain Res 11:281–301

    Google Scholar 

  • Damas H (1944) Recherches sur le développement de Lampetra fluviatilis L. Contribution à l'étude de la céphalogenèse des vertébrés. Arch Biol (Paris) 55:1–284

    Google Scholar 

  • De Miguel E, Anadón R (1987) The development of retina and the optic tectum of Petromyzon marinus L. A light microscopic study. J Hirnforsch 28:445–456

    Google Scholar 

  • De Miguel E, Rodicio MC, Anadón R (1989) Ganglion cells and retinopetal fibers of the larval lamprey retina: an HRP study. Neurosci Lett 106:1–6

    Google Scholar 

  • De Miguel E, Rodicio MC, Anadón R (1990) Organization of the visual system in larval lampreys: an HRP study. J Comp Neurol 302:529–542

    Google Scholar 

  • Ebbesson SOE, Meyer DL (1981) Efferents to the retina have multiple sources in teleost fish. Science 214:924–926

    Google Scholar 

  • Ebbesson SOE, Meyer DL (1989) Retinopetal cells exist in the optic tectum of the steelhead trout. Neurosci Lett 106:95–98

    Google Scholar 

  • Ekström P (1984) Central neural connections of the pineal organ and retina in the teleost Gasterosteus aculeatus L. J Comp Neurol 226:321–335

    Google Scholar 

  • Ferguson JL, Mulvany PJ, Brauth SE (1978) Distribution of neurons projecting to the retina of Caiman crocodilus. Brain Behav Evol 15:294–306

    Google Scholar 

  • Fritzsch B, Collin SP (1990) Dendritic distibution of two populations of ganglion cells and the retinopetal fibers in the retina of the silver lamprey (Ichthyomyzon unicuspis). Visual Neurosci 4:533–545

    Google Scholar 

  • González MJ, Anadón R (1992) Primary projections of the lateral line nerves in larval sea lamprey, Petromyzon marinus L. An HRP study. J Hirnforsch 33:185–194

    Google Scholar 

  • González MJ, Anadón R (1994) Central projections of the octaval nerve in larval lamprey: an HRP study. J Brain Res 35:181–189

    Google Scholar 

  • Hardisty MW, Potter IC (1971) The behaviour, ecology and growth of larval lampreys. In Hardisty MW, Potter IC (eds) The biology of lampreys, vol 1. Academic Press, London, pp85–125

    Google Scholar 

  • Heaton MB, Moody SA, Kosier ME (1978) Peripheral innervation by migrating neuroblast in the chick embryo. Neurosci Lett 10:55–59

    Google Scholar 

  • Homma S (1978) Organization of the trigeminal motor nucleus before and after metamorphosis in lampreys. Brain Res 140:33–44

    Google Scholar 

  • Hughes TE, Hall WC (1986) The transneuronal transport of horseradish peroxidase in the visual system of the frog (Rana pipiens). Neuroscience 17:507–518

    Google Scholar 

  • Leonhard H (1980) Ependym und circumventriculäre Organe. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie des Menschen, vol 4. Nervensystem, Part 10, Neuroglia I. Springer, Berlin Heidelberg New York, pp 177–666

    Google Scholar 

  • Meves A (1973) Elektronenmikroskopische Untersuchungen über die Zytoarchitektur des Gehirns von Branchiostoma lanceolatum. Z Zellforsch 130:511–532

    Google Scholar 

  • Meyer DL, Ebbesson SOE (1981) Retinofugal and retinopetal connections in the upsidedown catfish (Synodontis nigriventris). Cell Tissue Res 218:389–401

    Google Scholar 

  • Meyer DL, Fiebig E, Ebbesson SOE (1981) A note in the reciprocal connections between the retina and the brain in the puffer fish (Tetraodon fluviatilis). Neurosci Lett 23:111–115

    Google Scholar 

  • Meyer DL, Gerwerzhagen K, Fiebig E, Ahlswede F, Ebbesson SOE (1983) An isthmo-optic system in a bony fish. Cell Tissue Res 231:129–133

    Google Scholar 

  • Nakao T, Ishizawa A (1987) Development of the spinal nerves in the lamprey. I. Rohon-Beard cells and interneurons. J Comp Neurol 256:342–355

    Google Scholar 

  • Ooi EC, Youson JH (1976) Growth of the opisthonephric kidney during larval life in the anadromous sea lamprey, Petromyzon marinus L. Can J Zool 54:1449–1458

    Google Scholar 

  • Pombal MA, Rodicio MC, Anadón R (1994) Development and organization of the ocular motor nuclei in the larval sea lamprey Petromyzon marinus L.: an HRP study. J Comp Neurol 341:393–406

    Google Scholar 

  • Purvis HA (1979) Variations in growth, age at transformation, and sex ratio of sea lampreys re-established in chemically treated tributaries of the upper Great Lakes. Great Lakes Fish Commun Tech Rep 35:1–36

    Google Scholar 

  • Repérant J, Vesselkin NP, Ermakova TV, Kenigfest NB, Kosareva AA (1980) Radioautographic evidence for both orthograde and retrograde axonal transport of labeled compounds after intraocular injection of [3H] proline in the lamprey (Lampetra fluviatilis). Brain Res 200:179–183

    Google Scholar 

  • Rodicio MC, De Miguel E, Pombal MA, Anadón R (1992) The origin of trochlear motoneurons in the larval sea lamprey, Petromyzon marinus L. An HRP study. Neurosci Lett 138:19–22

    Google Scholar 

  • Rubinson K (1990) The developing visual system and metamorphosis in the lamprey. J Neurobiol 21:1123–1135

    Google Scholar 

  • Rubinson K, Cain H (1989) Neural differentiation in the retina of the larval sea lamprey (Petromyzon marinus). Visual Neurosci 3:241–248

    Google Scholar 

  • Rubinson K, Ripps H, Witkovsky P, Kennedy MC (1977) Retinal development in the lamprey, Petromyzon marinus. Soc Neurosci Abstr 3:575

    Google Scholar 

  • Ruiz MS, Anadón R (1989) Some observations on the fine structure of the Rohde cells of the spinal cord of the Amphioxus, Branchiostoma lanceolatum (Cephalochordata). J Hirnforsch 30:672–677

    Google Scholar 

  • Rusoff AC, Hapner SJ (1990) Development of retinopetal projections in the cichlid fish, Herotilapia multiespinosa. J Comp Neurol 294:431–442

    Google Scholar 

  • Schnyder H, Künzle H (1983) The retinopetal system in the turtle Pseudemys scripta elegans. Cell Tissue Res 234:219–224

    Google Scholar 

  • Schober W (1964) Vergleichend-anatomische Untersuchungen am Gehirn der Larven und adulten Tiere von Lampetra fluviatilis (Linné, 1758) und Lampetra planeri (Bloch, 1784). J Hirnforsch 7:107–209

    Google Scholar 

  • Schütte M, Weiler R (1988) Mesencephalic innervation of the turtle retina by a single serotonin-containing neuron. Neurosci Lett 91:289–294

    Google Scholar 

  • Tello JF (1923) Les différenciations neuronales dans l'embryon du poulet, pendant les premiers jours de l'incubation. Trav Lab Rech Biol Univ Madrid 21:1–93

    Google Scholar 

  • Tretjakoff DK (1916) The sense organs of the lamprey (Lampetra fluviatilis). University of Novorossijsk, Odessa

    Google Scholar 

  • Uchiyama H (1989) Centrifugal pathways to the retina: influence of the optic tectum. Visual Neurosci 3:183–206

    Google Scholar 

  • Vanegas H, Amat J, Essayag-Millan E (1973) Electrophysiological evidence of tectal efferents to the fish eye. Brain Res 54:309–313

    Google Scholar 

  • Vesselkin NP, Ermakova TV, Repérant J, Kosareva AA, Kenigfest N (1980) The retinofugal and retinopetal systems in Lampetra fluviatilis. An experimental study using radioautographic and HRP methods. Brain Res 195:453–460

    Google Scholar 

  • Vesselkin NP, Repérant J, Kenigfest NB, Miceli D, Ermakova TV, Rio JP (1984) An anatomical and electrophysiological study of the centrifugal visual system in the lamprey (Lampetra fluviatilis). Brain Res 292:41–56

    Google Scholar 

  • Vesselkin NP, Repérant J, Kenigfest NB, Rio JP, Miceli D, Shupliakov OV (1989) Centrifugal innervation of the lamprey retina. Light- and electron microscopic and electrophysiological investigations. Brain Res 493:51–65

    Google Scholar 

  • West RG (1972) Superficial warming of epoxy blocks for cutting of 25–150 μm sections to be resectioned in the 10–90 nm range. Stain Technol 47:201–204

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Biología Fundamental, Universidad de Santiago de Compostela, E-15706, Santiago de Compostela, Spain

    María Celina Rodicio & Ramón Anadón

  2. Departamento de Biología Celular y Molecular, Universidad de La Coruña, E-15071, La Coruña, Spain

    Manuel A. Pombal

Authors
  1. María Celina Rodicio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manuel A. Pombal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ramón Anadón
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodicio, M.C., Pombal, M.A. & Anadón, R. Early development and organization of the retinopetal system in the larval sea lamprey, Petromyzon marinus L.. Anat Embryol 192, 517–526 (1995). https://doi.org/10.1007/BF00187182

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00187182

Key words

Search

Navigation