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.
Abbreviations
- LLS:
-
Lateral line system
- PLLN:
-
Posterior lateral line nerve
References
Akoev GN, Muraveiko VM (1984) Physiological properties of lateral line receptors of the lamprey. Neurosci Lett 49:171–173
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 619–641
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 1–115
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 501–526
Bodznick D, Northcutt RG (1981) Electroreception in lampreys: evidence that the earliest vertebrates were electroreceptive. Science 212:465–467
Braun CB (1996) The sensory biology of the living jawless fishes: a phylogenetic assessment. Brain Behav Evol 48:262–276
Cahn PH, Shaw E (1963) Schooling fishes: the role of sensory factors. Anim Behav 11:405–406
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 129–166
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 553–586
Coombs S, Braun CB, Donovan B (2001) The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. J Exp Biol 204:337–348
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 198:2581–2591
Dijkgraaf S (1963) The functioning and significance of the lateral-line organs. Biol Rev 38:51–105
Gonzalez MJ, Anadon R (1992) Primary projections of the lateral line nerves in larval sea lamprey, Petromyzon marinus L—an HRP study. J Hirnforsch 33:185–194
Grillner S, Parker D, El Manira A (1998) Vertebrate locomotion—a lamprey perspective. Ann NY Acad Sci 860:1–18
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 85–127
Janssen J, Coombs S, Pride S (1990) Feeding and orientation of mottled sculpin, Cottus bairdi, to water jets. Environ Biol Fishes 29:43–50
Johnston JB (1905) The cranial nerve components of Petromyzon. Morphol Jahrb 34:149–203
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 83–130
Kanter MJ, Coombs S (2003) Rheotaxis and prey detection in uniform currents by Lake Michigan mottled sculpin (Cottus bairdi). J Exp Biol 206:59–70
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 276:245–252
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 295:277–289
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–P13
Kroese ABA, Schellart NAM (1992) Velocity- and acceleration-sensitive units in the trunk lateral line of the trout. J Neurophysiol 68:2212–2221
Lane EB, Whitear M (1982) Sensory structure at the surface of fish skin. II. Lateralis system. Zool J Linn Soc (Lond) 76:19–28
Lannoo MJ (1987) Neuromast topography in anuran amphibians. J Morphol 191:115–129
Montgomery JC, Macdonald JA (1987) Sensory tuning of lateral line receptors in Antarctic fish to the movement of planktonic prey. Science 235:195–196
Montgomery JC, Baker CF, Carton AG (1997) The lateral line can mediate rheotaxis in fish. Nature 389:960–963
Nelson SJ (1984) Fishes of the world. John Wiley & Sons, New York
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 York
Pitcher TJ, Partridge BL, Wardle CS (1976) A blind fish can school. Science 194:963–965
Pohlmann K, Atema J, Breithaupt T (2004) The importance of the lateral line in nocturnal predation of piscivorous catfish. J Exp Biol 207:2971–2978
Ronan M, Northcutt RG (1987) Primary projections of the lateral line nerves in adult lampreys. Brain Behav Evol 30:62–61
Rovainen CM (1982) Neurophysiology. In: Hardisty MW, Potter IC (eds) The biology of lampreys. Academic, London, pp 1–136
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 174:539–549
van Netten SM (2006) Hydrodynamic detection by cupulae in a lateral line canal: functional relations between physics and physiology. Biol Cybern 94:67–85
van Netten SM, Kroese ABA (1987) Laser interferometric measurements on the dynamic behavior of the cupula in the fish lateral line. Hear Res 29:55–61
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 York
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
Weissert R, Campenhausen C (1981) Discrimination between stationary objects by the blind cave fish Anoptichthys jordani (Characidae). J Comp Physiol A 143:375–381
Yamada Y (1973) Fine structure of the ordinary lateral line organ. I. The neuromast of lamprey, Entosphenus japonicus. J Ultrastruct Res 43:1–17
Young JZ (1935) The photoreceptors of lampreys I. Light-sensitive fibres in the lateral line nerves. J Exp Biol 12:229–238
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gelman, S., Ayali, A., Tytell, E.D. et al. Larval lampreys possess a functional lateral line system. J Comp Physiol A 193, 271–277 (2007). https://doi.org/10.1007/s00359-006-0183-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-006-0183-9