Electroreception pp 112-131 | Cite as
Ontogeny of Electroreceptors and Their Neural Circuitry
4. Summary
Ontogenetic studies provide a key to understanding the organization of different classes of sensory receptors, their distribution on the body, and their innervation. This is particularly true for the lateral line system of fishes and amphibians, as one class of sensory receptors, electroreceptors, was lost and then regained at a later time in two groups of teleost fishes. There are extensive descriptive and experimental studies documenting that primitive electroreceptors, that is, nonteleost ampullary organs, arise from lateral line placodes that generate one or more lines of neuromasts and the lateral line nerve that innervates these receptors. Ampullary organ and neuromast primordia arise from lateral and central zones, respectively, of sensory ridges, which form by the elongation of the lateral line placodes. In contrast to primitive electroreceptors, the embryonic origin of the reevolved ampullary organs and the newly evolved tuberous electroreceptors in teleosts is uncertain. It has been claimed that ampullary organs in catfishes develop from lateral line placodes, whereas ampullary and tuberous organs in gymnotids are claimed to develop from general ectoderm. Clearly, experimental studies are needed to resolve these different interpretations.
Almost nothing is known regarding the genetic basis for the induction and morphogenesis of either primitive or derived (teleost) electroreceptors. Similarly, there are no existing descriptions of the development of the central electroreceptive centers in taxa with primitive electroreceptors, and very little is known regarding the development of these centers and pathways in electroreceptive teleosts.
Keywords
Lateral Line Embryonic Origin Lateral Line System Electrosensory Lateral Line Lobe Posterior Lateral LinePreview
Unable to display preview. Download preview PDF.
References
- Allis EP (1889) The anatomy and development of the lateral line system in Amia calva. J Morphol 2:463–566.CrossRefGoogle Scholar
- Armstrong PB, Child JS (1962) Stages in the Development of Ictalurus Nebulosus. Syracuse, NY: Syracuse University Press.Google Scholar
- Baker CVH, Bronner-Fraser M (2001) Vertebrate cranial placodes. I. Embryonic induction. Dev Biol 232:1–61.PubMedCrossRefGoogle Scholar
- Beckwith CJ (1907) The early development of the lateral line system of Amia calva. Biol Bull 14:23–28.Google Scholar
- Bell CC, Szabo T (1986) Electroreception in mormyrid fish: central anatomy. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 375–422.Google Scholar
- Bemis WE, Northcutt RG (2004) Development of the lateral line system of the paddlefish Polyodon spathula (Actinopterygii: Acipenseriformes). J Morphol 260:277.Google Scholar
- Bensouilah M, Schugardt C, Roesler R, Kirschbaum F, Denizot J-P (2002) Larval electroreceptors in the epidermis of mormyrid fish: I. Tuberous organs of type A and B. J Comp Neurol 447:309–322.PubMedCrossRefGoogle Scholar
- Bever MM, Borgens RB (1991a) The regeneration of electroreceptors in Kryptopterus. J Comp Neurol 309:200–217.PubMedCrossRefGoogle Scholar
- Bever MM, Borgens RB (1991b) Patterning in the regeneration of electroreceptors in the fin of Kryptopterus. J Comp Neurol 309:218–230.PubMedCrossRefGoogle Scholar
- Bodznick D, Boord RL (1986) Electroreception in chondrichthyes: central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 225–256.Google Scholar
- Braford MR Jr. (1986) African knifefishes: the xenomystines. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 453–464.Google Scholar
- Bullock TH, Heiligenberg W (eds) (1986) Electroreception. New York: John Wiley & Sons.Google Scholar
- Bullock TH, Bodznick DA, Northcutt RG (1983) The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive vertebrate sense modality. Brain Res Rev 6:25–46.CrossRefGoogle Scholar
- Carr CE, Maler L (1986) Electroreception in gymnotiform fish: central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 319–374.Google Scholar
- Coombs S, Janssen J, Webb JF (1988) Diversity of lateral line systems: evolutionary and functional considerations. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds), Sensory Biology of Aquatic Animals. New York: Springer-Verlag, pp. 553–593.Google Scholar
- Coombs S, Görner P, Münz H (eds) (1989) The Mechanosensory Lateral Line: Neurobiology and Evolution. New York: Springer-Verlag.Google Scholar
- Denizot JP, Libouban S (1985) New formation of sensory cells in the tuberous organ (electroreceptor) of Brienomyrus niger (Mormyridae) induced by transection of afferent nerve. Int J Dev Neurosci 3:323–330.CrossRefGoogle Scholar
- Disler NN (1971) Lateral Line Sense Organs and Their Importance in Fish Behavior (trans Mills H, Yariv M), Mills H (ed). Jerusalem Keter Press.Google Scholar
- Disler NN (1977) The Lateral Line System Sense Organs of Sharks. Moscow: Science Publications.Google Scholar
- Finger TE (1986) Electroreception in catfish: behavior, anatomy, and electrophysiology In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 287–317.Google Scholar
- Fritzsch B, Bolz D (1986) On the development of electroreceptive ampullary organs of Triturus alpestris (Amphibia: Urodela). Amphibia Reptilia 7:1–9.Google Scholar
- Fritzsch B, Münz H (1986) Electroreception in amphibians. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 483–496.Google Scholar
- Gibbs MA, Northcutt RG (2004) Development of the lateral line system in the shovelnose sturgeon. Brain Behav Evol 64:70–84.PubMedCrossRefGoogle Scholar
- Haugedé-Carré F, Kirschbaum F, Szabo T (1977) On the development of the gigantocerebellum in the mormyrid fish Pollimyrus (Marcusenius) isidori. Neursci Lett 6: 209–213.CrossRefGoogle Scholar
- Holmgren N (1940) Studies on the head in fishes; embryological, morphological, and phylogenetical researches. Acta Zool 21:51–267.Google Scholar
- Johnson SE (1917) Structure and development of the sense organs of the lateral canal system of Selachians (Mustelus canis and Squalus acanthias). J Comp Neurol 28:1–74.CrossRefGoogle Scholar
- Kirschbaum F, Denizot J-P (1975) Sur la différenciation des électrorécepteurs chez Marcusenius sp. (Mormyrides) et Eigenmannia virescens (Gymnotides), poissons électriques à faible décharge. CR Acad Sci Paris 281:419–422.Google Scholar
- Landacre FL, Conger AC (1913) The origin of the lateral line primordia in Lepidosteus osseus. J Comp Neurol 23:575–633.Google Scholar
- Lannoo MJ, Lannoo SJ (1996) Development of the electrosensory lateral line lobe in the channel catfish, Ictalurus punctatus, with reference to the onset of swimming and feeding behaviors. Mar Fresh Behav Physiol 28:45–53.CrossRefGoogle Scholar
- Lannoo MJ, Vischer HA, Maler L (1990) Development of the electrosensory nervous system of Eigenmannia (Gymnotiformes): II. The electrosensory lateral line lobe, midbrain, and cerebellum. J Comp Neurol 294:37–58.PubMedCrossRefGoogle Scholar
- Lannoo MJ, Maler L, Hawkes R (1992) Zebrin II distinguishes the ampullary organ receptive map from the tuberous organ receptive maps during development in the teleost electrosensory lateral line lobe. Brain Res 586:176–180.PubMedCrossRefGoogle Scholar
- Leyhausen C, Kirschbaum F, Szabo T, Erdelen M (1987) Differential growth in the brain of the weakly electric fish, Apteronotus leptorhynchus (Gynotiformes), during ontogenesis. Brain Behav Evol 30:230–248.PubMedGoogle Scholar
- McCormick CA (1982) The organization of the octavolateralis area in actinopterygian fishes: a new interpretation. J Morphol 171:159–181.CrossRefGoogle Scholar
- Metcalfe WK (1985) Sensory neuron growth cones comigrate with posterior lateral line primordial cells in zebrafish. J Comp Neurol 238:218–224.PubMedCrossRefGoogle Scholar
- Metscher BD, Northcutt RG, Gardiner DM, Bryant SV (1997) Homeobox genes in axolotl lateral line placodes and neuromasts. Dev Genes Evol 207:287–295.CrossRefGoogle Scholar
- New JG (1997) The evolution of vertebrate electrosensory systems. Brain Behav Evol 50:244–252.PubMedGoogle Scholar
- Nikolskaya MP (1983) Development of the ampullar electroreceptor system in the ontogeny of Polyodon and Acipenseridae. Akad Nauk USSR 268:474–477.Google Scholar
- Northcutt RG (1986) Electroreception in nonteleost bony fishes. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 257–285.Google Scholar
- Northcutt RG (1989) The phylogenetic distribution and innervation of craniate mechanoreceptive lateral lines. In: Coombs S, Görner P, Münz H (eds), The Mechanosensory Lateral Line: Neurobiology and Evolution. New York: Springer-Verlag, pp. 17–78Google Scholar
- Northcutt RG (1997) Evolution of gnathostome lateral line ontogenies. Brain Behav Evol 50:25–37.PubMedGoogle Scholar
- Northcutt RG (2003) Development of the lateral line system in the channel catfish. In: Browman HI, Skiftesvik AB (eds), The Big Fish Bang. Proceedings of the 26th Annual Larval Fish Conference. Bergen, Norway: Institute of Marine Research, pp. 137–159.Google Scholar
- Northcutt RG, Bemis WE (1993) Cranial nerves of the coelacanth, Latimeria chalumnae [Osteichthyes: Sarcoptergii: Actinistia], and comparisons with other Craniata. Brain Behav Evol 42(S1):1–76.PubMedGoogle Scholar
- Northcutt RG, Brandle K (1995) Development of branchiomeric and lateral line nerves in the axolotl. J Comp Neurol 355:427–454.PubMedCrossRefGoogle Scholar
- Northcutt RG, Vischer HA (1988) Eigenmannia possesses autapomorphic rami of the anterior lateral line nerves. Soc Neurosci Abstr 14:54.Google Scholar
- Northcutt RG, Catania KC, Criley BB (1994) Development of lateral line organs in the axolotl. J Comp Neurol 340:480–514.PubMedCrossRefGoogle Scholar
- Northcutt RG, Brandle K, Fritzsch B (1995) Electroreceptors and mechanosensory lateral line organs arise from single placodes in axolotls. Dev Biol 168:358–373.PubMedCrossRefGoogle Scholar
- Northcutt RG, Holmes PH, Catania KC, Luer CA (1997) Lateral line system development in an elasmobranch, Raja eglanteria. Soc Neurosci Abstr 23:2380.Google Scholar
- Pehrson T (1949) The ontogeny of the lateral line system in the head of dipnoans. Acta Zool 30:153–182.CrossRefGoogle Scholar
- Piotrowski T, Northcutt RG (1996) The cranial nerves of the Senegal bichir, Polypterus senegalus [Osteichthyes: Actinopterygii: Caldistia]. Brain Behav Evol 47:55–102.PubMedGoogle Scholar
- Ronan M (1986) Electroreception in cyclostomes. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 209–224.Google Scholar
- Roth A (1986) Afferent fibers induce electroreceptors in the skin of fish. Naturwissenschaften 73:264–266.PubMedCrossRefGoogle Scholar
- Roth A (1993) Regenerative outgrowth and distribution of the electroreceptive nerve fibers in the catfish Kryptopterus. J Comp Neurol 328:473–484.PubMedCrossRefGoogle Scholar
- Roth A (1994) Development of the electrosensory system. Naturwissenschaften 81:269–272.Google Scholar
- Ruud G (1920) Uber Hautsinnesorgane bei Spinax niger Bon. Zool Jahrb Anat Ontogen 41:459–546.Google Scholar
- Sahly I, Andermann P, Petit C (1999) The zebrafish eya1 gene and its expression pattern during embryogenesis. Dev Genes Evol 209:399–410.PubMedCrossRefGoogle Scholar
- Schlosser G (2002a) Development and evolution of lateral line placodes in amphibians. I. Development. Zoology 105:119–146.PubMedCrossRefGoogle Scholar
- Schlosser G (2002b) Development and evolution of lateral line placodes in amphibians. II. Evolutionary diversification. Zoology 105:177–193.PubMedCrossRefGoogle Scholar
- Schlosser G, Northcutt RG (2000) Development of neurogenic placodes in Xenopus laevis. J Comp Neurol 418:121–146.PubMedCrossRefGoogle Scholar
- Song J, Northcutt RG (1991) The primary projections of the lateral line nerves of the Florida gar, Lepisosteus platyrhincus. Brain Behav Evol 37:38–63.PubMedGoogle Scholar
- Srivastava CBL, Seal M (1981) Electroreceptors in Indian catfish teleosts. Adv Physiol 31:1–11.Google Scholar
- Stone LS (1922) Experiments on the development of the cranial ganglia and the lateral line sense organs in Amblystoma punctatum. J Exp Zool 35:421–496.CrossRefGoogle Scholar
- Vischer HA (1989a) The development of lateral-line receptors in Eigenmannia (Teleostei, Gymnotiformes). I. The mechanoreceptive lateral-line system. Brain Behav Evol 33: 205–222.PubMedGoogle Scholar
- Vischer HA (1989b) The development of lateral-line receptors in Eigenmannia (Teleostei, Gymnotiformes). II. The electroreceptive lateral-line system. Brain Behav Evol 33: 223–236.PubMedGoogle Scholar
- Vischer HA (1995) Electroreceptor development in the electric fish Eigenmannia: a histological and ultrastructural study. J Comp Neurol 360:81–100.PubMedCrossRefGoogle Scholar
- Vischer HA, Lannoo MJ, Heiligenberg W (1989) Development of the electrosensory nervous system in Eigenmannia (Gymnotiformes): I. The peripheral nervous system. J Comp Neurol 290:16–40.PubMedCrossRefGoogle Scholar
- Webb JF (1989a) Developmental constraints and evolution of the lateral line system in teleost fishes. In: Coombs S, Görner P, Münz H (eds), The Mechanosensory Lateral Line: Neurobiology and Evolution. New York: Springer-Verlag, pp. 79–97Google Scholar
- Webb JF (1989b) Gross morphology and evolution of the mechanoreceptive lateral-line system in teleost fishes. Brain Behav Evol 33:34–53.PubMedGoogle Scholar
- Winklbauer R, Hausen P (1983) Development of the lateral line system in Xenopus laevis. I. Normal development and cell movement in the supraorbital system. J Embryol Exp Morphol 76:265–281.PubMedGoogle Scholar
- Zakon HH (1984) Postembryonic changes in the peripheral electrosensory system of a weakly electric fish: addition of receptor organs with age. J Comp Neurol 228:557–570.PubMedCrossRefGoogle Scholar
- Zakon HH (1986) The electroreceptive periphery. In: Bullock TH, Heiligenberg W (eds), Electroreception. New York: John Wiley & Sons, pp. 103–156.Google Scholar