Larval lampreys possess a functional lateral line system
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Abstract
Morphology of larval lampreys’ neuromasts was found to be very similar to that of adults. Activity in the lateral line nerve, elicited by a vibrating ball, indicated a functional lateralis system. Analysis revealed at least two populations of afferents, responding to opposite directions of water flow, with adapting responses. The response magnitude increased monotonically with stimulus amplitude. Larval lampreys’ neuromasts were less sensitive than those of teleosts. At low frequencies the response showed a phase lead of 200–220° with respect to the maximum of the ball displacement and a gain that was approximately linearly proportional to frequency.
Keywords
Lateral line Mechanoreception Neuromasts Ammocoetes LocomotionAbbreviations
- LLS
Lateral line system
- PLLN
Posterior lateral line nerve
Notes
Acknowledgments
We would like to thank Mr Timothy Maugel (University of Maryland, Electron Microscopy Laboratory) for assistance with SEM, Dr Tim Kiemel for help with the data analysis, and Dr Christopher Braun (Hunter College, CUNY) for valuable discussion. Experimental procedures were in compliance with the University of Maryland IACUC regulations. This work was supported by NIH grant 1RO1NS054271 to AHC.
References
- Akoev GN, Muraveiko VM (1984) Physiological properties of lateral line receptors of the lamprey. Neurosci Lett 49:171–173PubMedCrossRefGoogle Scholar
- Bleckmann H (1988) Prey identification and prey localization in surface-feeding fish and fishing spiders. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, Berlin Heidelberg New York, pp 619–641Google Scholar
- Bleckmann H (1994) Reception of hydrodynamic stimuli in aquatic and semiaquatic animals. In: Rathmayer W (ed) Progress in zoology. Gustav Fischer, Stuttgart, Jena, New York, pp 1–115Google Scholar
- Bleckmann H, Tittel G, Blubaum-Gronau E (1989) The lateral line system of surface-feeding fish: anatomy, physiology, and behavior. In: Coombs S, Gorner P, Munz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, Berlin Heidelberg New York, pp 501–526Google Scholar
- Bodznick D, Northcutt RG (1981) Electroreception in lampreys: evidence that the earliest vertebrates were electroreceptive. Science 212:465–467PubMedCrossRefGoogle Scholar
- Braun CB (1996) The sensory biology of the living jawless fishes: a phylogenetic assessment. Brain Behav Evol 48:262–276PubMedGoogle Scholar
- Cahn PH, Shaw E (1963) Schooling fishes: the role of sensory factors. Anim Behav 11:405–406CrossRefGoogle Scholar
- Cohen AH (1988) Evolution of the vertebrate central pattern generator for locomotion. In: Cohen AH, Rossignol S, Grillner S (eds) Neural control of rhythmic movements in vertebrates. Wiley, New York, pp 129–166Google 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. Springer, Berlin Heidelberg New York, pp 553–586Google Scholar
- Coombs S, Braun CB, Donovan B (2001) The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. J Exp Biol 204:337–348PubMedGoogle Scholar
- Deliagina TG, Ullen F, Gonzalez MJ, Ehrsson H, Orlovsky GN, Grillner S (1995) Initiation of locomotion by lateral-line photoreceptors in lamprey—behavioral and neurophysiological studies. J Exp Biol 198:2581–2591PubMedGoogle Scholar
- Dijkgraaf S (1963) The functioning and significance of the lateral-line organs. Biol Rev 38:51–105PubMedGoogle Scholar
- Gonzalez MJ, Anadon R (1992) Primary projections of the lateral line nerves in larval sea lamprey, Petromyzon marinus L—an HRP study. J Hirnforsch 33:185–194PubMedGoogle Scholar
- Grillner S, Parker D, El Manira A (1998) Vertebrate locomotion—a lamprey perspective. Ann NY Acad Sci 860:1–18PubMedCrossRefGoogle Scholar
- Hardisty MW, Potter IC (1971) The behaviour, ecology, and growth of larval lampreys. In: Hardisty MW, Potter IC (eds) The biology of lampreys. Academic, New York, pp 85–127Google Scholar
- Janssen J, Coombs S, Pride S (1990) Feeding and orientation of mottled sculpin, Cottus bairdi, to water jets. Environ Biol Fishes 29:43–50CrossRefGoogle Scholar
- Johnston JB (1905) The cranial nerve components of Petromyzon. Morphol Jahrb 34:149–203Google Scholar
- Kalmijn AJ (1988) Hydrodynamic and acoustic field detection. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, Berlin Heidelberg New York, pp 83–130Google Scholar
- Kanter MJ, Coombs S (2003) Rheotaxis and prey detection in uniform currents by Lake Michigan mottled sculpin (Cottus bairdi). J Exp Biol 206:59–70PubMedCrossRefGoogle Scholar
- Katori Y, Takasaka T, Ishikawa M, Tonosaki A (1994) Fine structure and lectin histochemistry of the apical surface of the free neuromast of Lampetra japonica. Cell Tissue Res 276:245–252Google Scholar
- Koyama H, Kishida R, Goris RC, Kusunoki T (1990) Organization of the primary projections of the lateral line nerves in the lamprey Lampetra japonica. J Comp Neurol 295:277–289PubMedCrossRefGoogle Scholar
- Kroese ABA, Schellart NAM (1987) Evidence for velocity-sensitive and acceleration-sensitive units in the trunk lateral line of the trout. J Physiol (Lond) 394:P13–P13Google Scholar
- Kroese ABA, Schellart NAM (1992) Velocity- and acceleration-sensitive units in the trunk lateral line of the trout. J Neurophysiol 68:2212–2221PubMedGoogle Scholar
- Lane EB, Whitear M (1982) Sensory structure at the surface of fish skin. II. Lateralis system. Zool J Linn Soc (Lond) 76:19–28CrossRefGoogle Scholar
- Lannoo MJ (1987) Neuromast topography in anuran amphibians. J Morphol 191:115–129CrossRefGoogle Scholar
- Montgomery JC, Macdonald JA (1987) Sensory tuning of lateral line receptors in Antarctic fish to the movement of planktonic prey. Science 235:195–196PubMedCrossRefGoogle Scholar
- Montgomery JC, Baker CF, Carton AG (1997) The lateral line can mediate rheotaxis in fish. Nature 389:960–963CrossRefGoogle Scholar
- Nelson SJ (1984) Fishes of the world. John Wiley & Sons, New YorkGoogle Scholar
- Northcutt GR (1989) The phylogenetic distribution and innervation of craniate mechanoreceptive lateral lines. In: Coombs S, Gorner P, Munz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, Berlin Heidelberg New YorkGoogle Scholar
- Pitcher TJ, Partridge BL, Wardle CS (1976) A blind fish can school. Science 194:963–965PubMedCrossRefGoogle Scholar
- Pohlmann K, Atema J, Breithaupt T (2004) The importance of the lateral line in nocturnal predation of piscivorous catfish. J Exp Biol 207:2971–2978PubMedCrossRefGoogle Scholar
- Ronan M, Northcutt RG (1987) Primary projections of the lateral line nerves in adult lampreys. Brain Behav Evol 30:62–61PubMedGoogle Scholar
- Rovainen CM (1982) Neurophysiology. In: Hardisty MW, Potter IC (eds) The biology of lampreys. Academic, London, pp 1–136Google Scholar
- Satou M, Takeuchi HA, Nishii J, Tanabe M, Kitamura S, Okumoto N, Iwata M (1994) Behavioral and electrophysiological evidences that the lateral line is involved in the inter-sexual vibrational communication of the himé salmon (landlocked red salmon, Oncorhynchus nerka). J Comp Physiol A 174:539–549Google Scholar
- van Netten SM (2006) Hydrodynamic detection by cupulae in a lateral line canal: functional relations between physics and physiology. Biol Cybern 94:67–85PubMedCrossRefGoogle Scholar
- van Netten SM, Kroese ABA (1987) Laser interferometric measurements on the dynamic behavior of the cupula in the fish lateral line. Hear Res 29:55–61PubMedCrossRefGoogle Scholar
- van Netten SM, Kroese ABA (1989) Dynamic behavior and micromechanical properties of the cupula. In: Coombs S, Gorner P, Munz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, Berlin Heidelberg New YorkGoogle Scholar
- Weeg MS, Bass AH (2002) Frequency response properties of lateral line superficial neuromasts in a vocal fish, with evidence for acoustic sensitivity. J Neurophysiol 88:1252–1262 PubMedGoogle Scholar
- Weissert R, Campenhausen C (1981) Discrimination between stationary objects by the blind cave fish Anoptichthys jordani (Characidae). J Comp Physiol A 143:375–381CrossRefGoogle Scholar
- Yamada Y (1973) Fine structure of the ordinary lateral line organ. I. The neuromast of lamprey, Entosphenus japonicus. J Ultrastruct Res 43:1–17PubMedCrossRefGoogle Scholar
- Young JZ (1935) The photoreceptors of lampreys I. Light-sensitive fibres in the lateral line nerves. J Exp Biol 12:229–238Google Scholar