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Mechanical filtering by the boundary layer and fluid–structure interaction in the superficial neuromast of the fish lateral line system

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Abstract

A great diversity of aquatic animals detects water flow with ciliated mechanoreceptors on the body’s surface. In order to understand how these receptors mechanically filter signals, we developed a theoretical model of the superficial neuromast in the fish lateral line system. The cupula of the neuromast was modeled as a cylindrical beam that deflects in response to an oscillating flow field. Its accuracy was verified by comparison with prior measurements of cupular deflection in larval zebrafish (Danio rerio). The model predicts that the boundary layer of flow over the body attenuates low-frequency stimuli. The fluid–structure interaction between this flow and the cupula attenuates high-frequency stimuli. The number and height of hair cell kinocilia and the dimensions of the cupular matrix determine the range of intermediate frequencies to which a neuromast is sensitive. By articulating the individual mechanical contributions of the boundary layer and the components of cupular morphology, this model provides the theoretical framework for understanding how a hydrodynamic receptor filters flow signals.

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Abbreviations

a :

radius of cupula at base

a s :

radius of a sphere

b m :

force coefficient for cupular material

b w :

force coefficient for fluid

c :

speed of sound in water

C :

integration constant

E m :

Young’s modulus of cupular matrix

F :

stimulus frequency

F b :

buoyant force

F e :

elastic force

F m :

inertial force

F a :

acceleration reaction

F u :

viscous drag

h h :

height of hair bundle

h c :

height of cupula

h k :

height of kinocilia

I :

second moment of area

k :

viscous drag coefficient

L :

hydrodynamic force coefficient

M :

bending moment

N :

number of hair cells

p :

distance between center of sphere and flat plate

q l :

linear spring bundle stiffness

q t :

torsion spring bundle stiffness

r :

distance from center of sphere

Re :

Reynolds number

S h :

sensitivity of cupula to local flow

S b :

sensitivity of local flow to freestream flow

S f :

sensitivity of cupula to freestream flow

S l :

Sensitivity of local flow to an oscillating sphere

S s :

sensitivity of cupula to oscillating sphere

St :

Strouhal number

t :

time

U :

flow velocity

U :

freestream velocity

U s :

flow velocity generated by an oscillating sphere

U s,lin :

linearized flow velocity generated by vibrating sphere

W :

sphere velocity

\( \hat{\user2{x}} \) :

unit vector along body

z :

position along height

\( \hat{\user2{z}} \) :

unit vector along height

β :

boundary layer flow velocity gradient

δ :

boundary layer thickness

μ:

dynamic viscosity of water

ν:

cupula deflection

νs :

cupula deflection by vibrating sphere

ρm :

density of cupular material

ρw :

density of fluid

ω:

angular rate of oscillation

References

  • Anderson EJ, McGillis WR, Grosenbaugh MA (2001) The boundary layer of swimming fish. J Exp Biol 204:81–102

    PubMed  CAS  Google Scholar 

  • Arkett SA, Mackie GO (1988) Hair cell mechanoreception in the jellyfish Aglantha digitale. J Exp Biol 135:329–342

    Google Scholar 

  • Batchelor GK (1967) An introduction to fluid dynamics. Cambridge University Press, New York

    Google Scholar 

  • van Bergeijk WA (1967) Introductory comments on lateral line function. In: Cahn PH (ed) Lateral line detectors. Indiana University Press, Bloomington, pp 73–81

    Google Scholar 

  • Bleckmann H (1994) Reception of hydrodynamic stimuli in aquatic and semiaquatic animals. Prog Zool 41:1–115

    Google Scholar 

  • Bone Q, Ryan KP (1978) Cupular sense organs in Ciona (Tunicata: Ascidiacea). J Zool Lond 186:417–429

    Google Scholar 

  • Budelmann BU (1989) Hydrodynamic receptor systems in invertebrates. In: Coombs S, Gorner P, Münz H (eds) The mechanosensory lateral line. Springer, Berlin, pp 607–631

    Google Scholar 

  • Budelmann BU, Bleckmann H (1988) A lateral line analogue in cephalopods: water waves generate microphonic potentials in the epidermal head lines of Sepia and Lolliguncula. J Comp Physiol A 164:1–5

    Article  PubMed  CAS  Google Scholar 

  • Cahn PH, Shaw E (1962) The first demonstration of lateral line cupulae in the Mugiliformes. Copeia 1962:109–114

    Article  Google Scholar 

  • Coombs S, Conley RA (1997) Dipole source localization by the mottled sculpin. 2. The role of lateral line excitation patterns. J Comp Physiol A 180:401–415

    Article  PubMed  CAS  Google Scholar 

  • Coombs S, Hasting M, Finneran J (1996) Modeling and measuring lateral line excitation patterns to changing dipole source locations. J Comp Physiol A 178:359–371

    Article  PubMed  CAS  Google Scholar 

  • Coombs S, Montgomery JC (1999) The enigmatic lateral line system. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York

    Google Scholar 

  • Coombs S, van Netten SM (2006) The hydrodynamics and structural mechanics of the lateral line system. In: Shadwick RE, Lauder GV (eds) Fish biomechanics. Elsevier, New York, pp 103–139

    Google Scholar 

  • Curcic-Blake B, van Netten SM (2006) Source location encoding in the fish lateral line canal. J Exp Biol 209:1548–1559

    Article  PubMed  Google Scholar 

  • Daniel TL (1981) Fish mucus: in situ measurements of polymer drag reduction. Biol Bull 160:376–382

    Article  Google Scholar 

  • Denton EJ, Gray JAB (1983) Mechanical factors in the excitation of clupeid lateral lines. Proc R Soc Lond 218:1–26

    Article  CAS  Google Scholar 

  • Denton EJ, Gray JAB (1982) The rigidity of fish and patterns of lateral line stimulation. Nature 297:679–681

    Article  PubMed  CAS  Google Scholar 

  • Devarakonda R, Barth FG, Humphrey JAC (1996) Dynamics of arthropod filiform hairs. IV. Motion in air and water. Proc R Soc Lond 351:933–946

    Google Scholar 

  • Dinklo T (2005) Mechno- and electrophysiological studies on cochlear hair cells and superficial lateral line cupulae. Doctoral dissertation, Neurobiophysics, University of Groningen

  • Flock A (1965) Electron microscopic and electrophysiological studies on the lateral line canal organ. Acta Otolaryngol Suppl 199:1–90

    Google Scholar 

  • Gere JM (2001) Mechanics of materials. Nelson Thornes Ltd, Cheltenham

    Google Scholar 

  • Harris GG, Frishkopf LS, Flock A (1970) Receptor potentials from hair cells of the lateral line. Science 167:76–79

    Article  PubMed  CAS  Google Scholar 

  • Harris GG, Milne DC (1966) Input-output characteristics of the lateral-line organs of Xenopus laevis. J Acoust Soc Am 40:32–42

    Article  PubMed  CAS  Google Scholar 

  • Hassan ES (1985) Mathematical analysis of the stimulus of the lateral line organ. Biol Cybern 52:23–36

    Article  PubMed  CAS  Google Scholar 

  • Highham TE, Day SW, Wainwright PC (2006) Multidimensional analysis of suction feeding performance in fishes: fluid speed, acceleration, strike accuracy and the ingested volume of water. J Exp Biol 209:2713–2725

    Article  Google Scholar 

  • Hofer B (1908) Studien ϋber die Hautsinnesorgane der Fische. I. Die funktion der seitenorgane bei den fischen. Ber Kgl Bayer Biol Versuchsstation München 1:115–164

    Google Scholar 

  • Howard J, Hudspeth AJ (1988) Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog saccular hair cell. Neuron 1:189–199

    Article  PubMed  CAS  Google Scholar 

  • Hudspeth AJ (1982) Extracellular current flow and the site of transduction by vertebrate hair cells. J Neurosci 2:1–10

    PubMed  CAS  Google Scholar 

  • Hudspeth AJ (1989) How the ear’s works work. Nature 341:397–404

    Article  PubMed  CAS  Google Scholar 

  • Hudspeth AJ, Corey DP (1977) Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci 74:2407–2411

    Article  PubMed  CAS  Google Scholar 

  • Hudspeth AJ, Jacobs R (1979) Stereocilia mediate transduction in vertebrate hair cells. Proc Natl Acad Sci 76:1506–1509

    Article  PubMed  CAS  Google Scholar 

  • Humphrey JAC, Devarakonda R, Iglesias I, Barth FG (1993) Dynamics of arthropod filiform hairs. I. Mathematical modeling of the hair and air motions. Philos Trans R Soc Lond B 340:423–444

    Article  Google Scholar 

  • Hussey RG, Good BJ, Reynolds JM (1967) Oscillation of two cylinders in liquid helium. Phys Fluids 10:89–95

    Article  CAS  Google Scholar 

  • Janssen J (2004) Lateral line sensory ecology. In: Emde GVD, Mogdans J, Kapoor BG (eds) The senses of fish: adaptations for the reception of natural stimuli. Kluwer, Boston, pp 231–264

    Google Scholar 

  • Jielof R, Spoor A, de Vries H (1952) The microphonic activity of the lateral line. J Physiol 116:137–157

    PubMed  CAS  Google 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, New York, pp 83–130

    Google Scholar 

  • Kalmijn AJ (1989) Functional evolution of lateral line and inner ear sensory systems. In: Coombs S, Gorner P, Münz H (eds) The mechanosensory lateral line. Springer, Berlin, pp 187–215

    Google Scholar 

  • Kelly JP, van Netten SM (1991) Topology and mechanics of the cupula in the fish lateral line. Variations of cupular structure and composition in three dimensions. J Morphol 207:23–36

    Article  PubMed  CAS  Google Scholar 

  • Kroese ABA, Schellart NAM (1987) Evidence for velocity and acceleration-sensitive units in the trunk lateral line of the trout. J Physiol 394:2212–2221

    Google Scholar 

  • Kroese ABA, van der Zalm JM, van den Bercken J (1978) Frequency response of the lateral-line organ of Xenopus laevis. Pfluegers Arch 375:167–175

    Article  CAS  Google Scholar 

  • Kroese ABA, van der Zalm JM, van den Bercken J (1980) Extracellular receptor potentials from the lateral-line organ of xenopus laevis. J Exp Biol 86:63–77

    Google Scholar 

  • Kuiper JW (1967) Frequency characteristics and functional significance of the lateral line organ. In: Cahn PH (ed) Lateral line detectors. Indiana University Press, Bloomington, pp 105–121

    Google Scholar 

  • Lamb H (1911) On the uniform motion of a sphere through a viscous fluid. Philos Mag 21:112

    Google Scholar 

  • Lamb H (1945) Hydrodynamics. Article 361. Dover, New York

    Google Scholar 

  • McHenry MJ, Lauder GV (2005) The mechanical scaling of coasting in zebrafish (Danio rerio). J Exp Biol 208:2289–2301

    Article  PubMed  Google Scholar 

  • McHenry MJ, van Netten SM (2007) The flexural stiffness of superficial neuromasts in the zebrafish (Danio rerio) lateral line. J Exp Biol 210:4244–4253

    Article  PubMed  Google Scholar 

  • Mogdans J, Krother S, Engelmann J (2004) Neurobiology of the fish lateral line: adaptations for the detection of hydrodynamic stimuli in running water. In: Emde GVD, Mogdans J, Kapoor BG (eds) The senses of fish: adaptations for the reception of natural stimuli. Narosa Publishing House, New Delhi, pp 265–287

    Google Scholar 

  • Montgomery J, Coombs S (1992) Physiological characterization of lateral line function in the antarctic fish Trematomus-Bernacchii. Brain Behav Evol 40:209–216

    Article  PubMed  CAS  Google Scholar 

  • Moore AMF, Cobb JLS (1986) Neurophysiological studies on the detection of mechanical stimuli in Ophiura ophiura. J Exp Mar Biol Ecol 104:125–141

    Article  Google Scholar 

  • Münz H (1979) Morphology and innervation of the lateral line system in Sarotherodon niloticus (L.) (Cichlidae, Teleostei). Zoomorphologie 93:73–86

    Article  Google Scholar 

  • Münz H (1985) Single unit activity in the peripheral lateral line system of the cichlid fish Sarotherodon niloticus L. J Comp Physiol A 157:555–568

    Article  Google Scholar 

  • Münz H, Claas B, Fritzsch B (1984) Electroreceptive and mechanoreceptive units in the lateral line of the axolotl Ambystoma-mexicanum. J Comp Physiol A 154:33–44

    Article  Google Scholar 

  • van Netten SM (1988) Laser interferometric microscope for the measurement of nanometer vibrational displacements of a light-scattering microscopic object. J Acoust Soc Am 83:1667–1674

    Article  Google Scholar 

  • van Netten SM (2006) Hydrodynamic detection by cupulae in a lateral line canal: functional relations between physics and physiology. Biol Cyber 94:67–85

    Article  Google Scholar 

  • van Netten SM, Kroese ABA (1987) Laser interferometric measurements on the dynamic behavior of the cupula in the fish lateral line. Hear Res 29:55–61

    Article  PubMed  Google Scholar 

  • Oseen, CW (1910) Über die Stokessche Formel und über eine verwandte Aufgabe in der Hydrodynamik. Ark Mat Astr Fys 6

  • Peleshanko S, Julian MD, Ornatska M, McConney ME, LeMieux MC, Chen N, Tucker C, Yang Y, Liu C, Humphrey JAC, Tsukruk VV (2007) Hydrogel-encapsulated microfabricated haircell mimicking fish cupulae neuromast. Adv Mater 19:2903–2909

    Article  CAS  Google Scholar 

  • Pozrikidis C (1997) Shear flow over a protuberance on a plane wall. J Eng Math 31:29–42

    Article  Google Scholar 

  • Sarpkaya T (1986) Force on a circular cylinder in viscous oscillatory flow at low Keulegan–Carpenter numbers. J Fluid Mech 165:61–71

    Article  Google Scholar 

  • Sato M (1962) Studies on the pit organs of fishes V. The structure and polysaccharide histochemistry of the cupula pit organ. Annot Zool Jpn 35:80–88

    Google Scholar 

  • Scharrer E (1932) Experiments on the function of the lateral-line organs in the larvae of Amblystoma punctatus. J Exp Zool 61:109–114

    Article  Google Scholar 

  • Schlichting H (1979) Boundary-layer theory. McGraw-Hill, New York

    Google Scholar 

  • Schulze FE (1861) Uber die Nervenendigung in den sogenannten Schleimkanälen der Fische und über entsprechende Organe der durch Kiemen athmenden Amphibien Arch Anat Pizysiol Lpz 759–769

  • Shatz LF (2005) Slender body method for slender prolate spheroids and hemispheroids on planes in linearized oscillatory flow. Phys Fluids 17:113603

    Article  CAS  Google Scholar 

  • Stokes GG (1851) On the effect if the internal friction of fluids on the motion of pendulums. Trans Camb Philos Soc 9:8–106

    Google Scholar 

  • Stuart JT (1963) Unsteady boundary layers. In: Rosenhead L (ed) Laminar boundary layers. Clarendon Press, Oxford, pp 349–407

    Google Scholar 

  • Teyke T (1988) Flow field, swimming velocity, and boundary layer: parameters which affect the stimulus for the lateral line organ in blind fish. J Comp Physiol A 163:53–61

    Article  PubMed  CAS  Google Scholar 

  • Teyke T (1990) Morphological differences in neuromasts of the blind cave fish Astyanax-Hubbsi and the sighted river fish Astyanax-Mexicanus. Brain Behav Evol 35:23–30

    Article  PubMed  CAS  Google Scholar 

  • Van Trump WJ, McHenry MJ (2008) Lateral line morphology and sensitivity in zebrafish larvae (Danio rerio). J Exp Biol 211:2105–2115

    Article  PubMed  Google Scholar 

  • Wakiya S (1961) Effect of a submerged object on a slow viscous flow. Res Rep Fac Eng Niigata Univ Jpn 10:15–24

    Google Scholar 

  • Wakiya S (1963) Effect of a plane wall on the impulsive motion of a sphere in a viscous fluid. J Phys Soc Jpn 19:1401–1408

    Article  Google Scholar 

  • Weast RC (1987) CRC handbook of chemistry and physics, vol 68

  • Wainwright SA, Biggs WD, Currey JD, Gosline JM (1976) Mechanical design in organisms. Princeton University Press, Princeton

    Google Scholar 

  • Williams RE, Hussey RG (1972) Oscillating cylinders and the Stokes’ paradox. Phys Fluids 15:2083–2088

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by National Science Foundation grants to MJM (IOS-0723288 and IOB-0509740). Although no experiments were performed for this work, we have complied with the “Principles of animal care”, publication no. 86-23, revised 1985 of the National Institute of Health, and also with the current laws of the USA and The Netherlands.

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Correspondence to Matthew J. McHenry.

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McHenry, M.J., Strother, J.A. & van Netten, S.M. Mechanical filtering by the boundary layer and fluid–structure interaction in the superficial neuromast of the fish lateral line system. J Comp Physiol A 194, 795–810 (2008). https://doi.org/10.1007/s00359-008-0350-2

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  • DOI: https://doi.org/10.1007/s00359-008-0350-2

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