The flexural stiffness of superficial neuromasts in the zebrafish (Danio rerio) lateral line

SUMMARY Superficial neuromasts are structures that detect water flow on the surface of the body of fish and amphibians. As a component of the lateral line system, these receptors are distributed along the body, where they sense flow patterns that mediate a wide variety of behaviors. Their ability to detect flow is governed by their structural properties, yet the micromechanics of superficial neuromasts are not well understood. The aim of this study was to examine these mechanics in zebrafish (Danio rerio) larvae by measuring the flexural stiffness of individual neuromasts. Each neuromast possesses a gelatinous cupula that is anchored to hair cells by kinocilia. Using quasi-static bending tests of the proximal region of the cupula, we found that flexural stiffness is proportional to the number of hair cells, and consequently the number of kinocilia, within a neuromast. From this relationship, the flexural stiffness of an individual kinocilium was found to be 2.4×10–20 N m2. Using this value, we estimate that the 11 kinocilia in an average cupula generate more than four-fifths of the total flexural stiffness in the proximal region. The relatively minor contribution of the cupular matrix may be attributed to its highly compliant material composition (Young's modulus of ∼21 Pa). The distal tip of the cupula is entirely composed of this material and is consequently predicted to be at least an order of magnitude more flexible than the proximal region. These findings suggest that the transduction of flow by a superficial neuromast depends on structural dynamics that are dominated by the number and height of kinocilia.

[1]  A. Hess.  DEVELOPMENTAL CHANGES IN THE STRUCTURE OF THE SYNAPSE ON THE MYELINATED CELL BODIES OF THE CHICKEN CILIARY GANGLION , 1965, The Journal of cell biology.

[2]  E. Hassan,et al.  On the discrimination of spatial intervals by the blind cave fish (Anoptichthys jordani) , 1986, Journal of Comparative Physiology A.

[3]  Sietse M. van Netten,et al.  Laser interferometric measurements on the dynamic behaviour of the cupula in the fish lateral line , 1987, Hearing Research.

[4]  J. Montgomery,et al.  The lateral line can mediate rheotaxis in fish , 1997, Nature.

[5]  Alfon B. A. Kroese,et al.  Sensory Transduction in Lateral Line Hair cells , 1989 .

[6]  E. Denton,et al.  Mechanical factors in the excitation of clupeid lateral lines , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[7]  J. Kelly,et al.  Topography and mechanics of the cupula in the fish lateral line. I. Variation of cupular structure and composition in three dimensions , 1991, Journal of morphology.

[8]  Geoffrey A. Manley.  Vertebrate Hair Cells , 2006 .

[9]  A. V. Grimstone,et al.  The Fine Structure of the Mesenteries of the Sea-Anemone Metridium senile , 1958 .

[10]  Ad. J. Kalmijn,et al.  Hydrodynamic and Acoustic Field Detection , 1988 .

[11]  Eric Schabtach,et al.  Anatomy of the posterior lateral line system in young larvae of the zebrafish , 1985, The Journal of comparative neurology.

[12]  D. Fawcett.  Cilia and Flagella , 1961 .

[13]  J. Webb.  Ontogeny and phylogeny of the trunk lateral line system in cichlid fishes , 1990 .

[14]  H. de Vries,et al.  The microphonic activity of the lateral line , 1952, The Journal of physiology.

[15]  W. Megill,et al.  The modulus of elasticity of fibrillin-containing elastic fibres in the mesoglea of the hydromedusa Polyorchis penicillatus , 2005, Journal of Experimental Biology.

[16]  Sheryl Coombs,et al.  The Mechanosensory Lateral Line , 1989 .

[17]  Michael Brand,et al.  Keeping and raising zebrafish , 2002 .

[18]  N A Schellart,et al.  Velocity- and acceleration-sensitive units in the trunk lateral line of the trout. , 1992, Journal of neurophysiology.

[19]  El-S. Hassan,et al.  Mathematical analysis of the stimulus for the lateral line organ , 1985, Biological Cybernetics.

[20]  G. Chapman.  Studies of the Mesogloea of Coelenterates: I. Histology and Chemical Properties , 1953 .

[21]  S. V. Netten,et al.  Dynamic Behavior and Micromechanical Properties of the Cupula , 1989 .

[22]  Rainer W Friedrich,et al.  Genetic Analysis of Vertebrate Sensory Hair Cell Mechanosensation: the Zebrafish Circler Mutants , 1998, Neuron.

[23]  A. Hudspeth,et al.  Directional cell migration establishes the axes of planar polarity in the posterior lateral-line organ of the zebrafish. , 2004, Developmental cell.

[24]  Jack Chen,et al.  Design and fabrication of artificial lateral line flow sensors , 2002 .

[25]  A J Hudspeth,et al.  Stereocilia mediate transduction in vertebrate hair cells (auditory system/cilium/vestibular system). , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[26]  T. Dinklo.  Mechano- and electrophysiological studies on cochlear hair cells and lateral line cupulae , 2005 .

[27]  Stephen A. Wainwright,et al.  Mechanical Design in Organisms , 2020 .

[28]  H. Münz,et al.  Functional Organization of the Lateral Line Periphery , 1989 .

[29]  G. Quinn,et al.  Experimental Design and Data Analysis for Biologists , 2002 .

[30]  J. Blaxter.  Cupular growth in herring neuromasts , 1984, Journal of the Marine Biological Association of the United Kingdom.

[31]  S. Baba,et al.  Flexural rigidity and elastic constant of cilia. , 1972, The Journal of experimental biology.

[32]  M. Sato.  Studies on the pit organs of fishes. V. The structure and polysaccharide histochemistry of the cupula of the pit organ , 1962 .

[33]  M. A. R. Koehl,et al.  Mechanical Diversity of Connective Tissue of the Body Wall of Sea Anemones , 1977 .

[34]  R. Northcutt.  The Phylogenetic Distribution and Innervation of Craniate Mechanoreceptive Lateral Lines , 1989 .

[35]  T. Takasaka,et al.  Fine structure of guinea pig vestibular kinocilium. , 1989, Acta oto-laryngologica.

[36]  John M. Gosline,et al.  Mechanics of Jet Propulsion in the Hydromedusan Jellyfish, Polyorchis Pexicillatus: I. Mechanical Properties of the Locomotor Structure , 1988 .

[37]  J. Gosline.  Connective Tissue Mechanics of Metridium Senile , 1971 .

[38]  Rainer W Friedrich,et al.  NompC TRP Channel Required for Vertebrate Sensory Hair Cell Mechanotransduction , 2003, Science.

[39]  S. Appelbaum,et al.  Scanning electron microscopic observations of the chemo- and mechanoreceptors of carp larvae (Cyprinus carpio) and their relationship to early behaviour , 1997 .

[40]  D. Raible,et al.  Organization of the lateral line system in embryonic zebrafish , 2000, The Journal of comparative neurology.

[41]  Heidi L. Rehm,et al.  TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells , 2004, Nature.

[42]  Nannan Chen,et al.  Hydrogel‐Encapsulated Microfabricated Haircells Mimicking Fish Cupula Neuromast , 2007 .

[43]  J. Fetcho,et al.  Laser Ablations Reveal Functional Relationships of Segmental Hindbrain Neurons in Zebrafish , 1999, Neuron.

[44]  S. Dijkgraaf.  Bau und Funktionen der Seitenorgane und des Ohrlabyrinths bei Fischen , 1952, Experientia.

[45]  Martha Denny,et al.  The lateral‐line system of the teleost, fundulus heteroclitus , 1937 .

[46]  A. Ghysen,et al.  Somatotopy of the lateral line projection in larval zebrafish. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[47]  H. Münz.  Morphology and innervation of the lateral line system inSarotherodon niloticus (L.) (cichlidae, teleostei) , 1979, Zoomorphologie.

[48]  S. Timoshenko.  History of strength of materials , 1953 .

[49]  A. Flock,et al.  ELECTRON MICROSCOPIC AND ELECTROPHYSIOLOGICAL STUDIES ON THE LATERAL LINE CANAL ORGAN. , 1964, Acta oto-laryngologica. Supplementum.

[50]  Y. Hiramoto,et al.  DIRECT MEASUREMENTS OF THE STIFFNESS OF ECHINODERM SPERM FLAGELLA , 1979 .

[51]  A. Flock,et al.  THE ULTRASTRUCTURE OF THE KINOCILIUM OF THE SENSORY CELLS IN THE INNER EAR AND LATERAL LINE ORGANS , 1965, The Journal of cell biology.

[52]  E. R. Cohen.  An Introduction to Error Analysis: The Study of Uncertainties in Physical Measurements , 1998 .

[53]  K. Takahashi.  Cilia and flagella. , 1984, Cell structure and function.

[54]  A. Flock,et al.  Transducing mechanisms in the lateral line canal organ receptors. , 1965, Cold Spring Harbor symposia on quantitative biology.

[55]  J. Webb,et al.  Postembryonic development of the cranial lateral line canals and neuromasts in zebrafish , 2003, Developmental dynamics : an official publication of the American Association of Anatomists.

[56]  Lee A. Fuiman,et al.  Function of the Free Neuromasts of Marine Teleost Larvae , 1989 .

[57]  J. Webb.  Neuromast morphology and lateral line trunk canal ontogeny in two species of cichlids: An SEM study , 1989, Journal of morphology.

[58]  E. Shaw,et al.  The First Demonstration of Lateral Line Cupulae in the Mugiliformes , 1962 .

[59]  L. Fuiman,et al.  Sensory development and concurrent behavioural changes in Atlantic croaker larvae , 1997 .

[60]  Y. Hiramoto,et al.  Flexural rigidity of echinoderm sperm flagella. , 1994, Cell structure and function.

[61]  A. J. Hudspeth,et al.  Stereocilia mediate transduction in vertebrate hair cells , 1979 .

[62]  T Teyke,et al.  Morphological differences in neuromasts of the blind cave fish Astyanax hubbsi and the sighted river fish Astyanax mexicanus. , 1990, Brain, behavior and evolution.

[63]  T. Teyke,et al.  Flow field, swimming velocity and boundary layer: parameters which affect the stimulus for the lateral line organ in blind fish , 1988, Journal of Comparative Physiology A.

[64]  C. Brokaw.  Direct measurements of sliding between outer doublet microtubules in swimming sperm flagella. , 1989, Science.

[65]  J. Nishii,et al.  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) , 1994, Journal of Comparative Physiology A.

[66]  S. V. van Netten.  Hydrodynamic detection by cupulae in a lateral line canal: functional relations between physics and physiology. , 2006, Biological cybernetics.