The Hydrodynamics and Structural Mechanics of the Lateral Line System

Publisher Summary This chapter summarizes some of the key biomechanical and hydrodynamic features of the lateral line system—especially as they pertain to the extraction and encoding of information relevant to the lives of fishes. Because the lateral line is an essentially an array of flow sensors, fluid dynamics plays a particularly significant role in shaping the response properties of octavolateralis system. The lateral line system is a primitive vertebrate sensory system, found exclusively in aquatic, anamniotic vertebrates. It is closely associated with a suite of octavolateralis sensory systems, which include the vestibular and auditory organs of the inner ear and the electro‐ and mechano‐sensory lateral line systems. The term ‘‘octavolateralis'’ is derived from the cranial nerves that innervate these systems and enter the brain in close proximity to one another. The paired organs of the inner ear are innervated by different branches of the eighth (octavo) cranial nerve, whereas the spatially distributed, multiple‐organ systems of the electro‐ and mechano‐sensory lateral line are innervated by as many as five different lateral line cranial nerves. Octavolateralis sensory functions are also intricately linked to the biomechanical effects of whole‐body or body part movements of fish, which can stimulate one or more octavolateralis systems of a nearby receiving fish to indicate the presence, identity, location, or intention of a predator, prey, or mate.

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

[2]  Ad. J. Kalmijn,et al.  Functional Evolution of Lateral Line and Inner Ear Sensory Systems , 1989 .

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

[4]  John C. Montgomery,et al.  Functional and Evolutionary Implications of Peripheral Diversity in Lateral Line Systems , 1992 .

[5]  Branislava Ćurčić-Blake,et al.  Rapid responses of the cupula in the lateral line of ruffe (Gymnocephalus cernuus) , 2005, Journal of Comparative Physiology A.

[6]  A. J. Hudspeth,et al.  Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the Bullfrog's saccular hair cell , 1988, Neuron.

[7]  A J Hudspeth,et al.  Ca2+ current–driven nonlinear amplification by the mammalian cochlea in vitro , 2005, Nature Neuroscience.

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

[9]  J. Montgomery,et al.  Comparing Octavolateralis Sensory Systems: What Can We Learn? , 2005 .

[10]  J. Webb,et al.  Developmental Constraints and Evolution of the Lateral Line System in Teleost Fishes , 1989 .

[11]  Sietse M. van Netten,et al.  Hydrodynamic detection by cupulae in a lateral line canal: functional relations between physics and physiology , 2005, Biological Cybernetics.

[12]  C. Geisler.  A model of stereociliary tip-link stretches , 1993, Hearing Research.

[13]  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.

[14]  T. Tricas,et al.  Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray , 2004, Journal of Experimental Biology.

[15]  P Tsang.  Laser interferometric flow measurements in the lateral line organ , 1997 .

[16]  J. Pickles,et al.  Morphology and cross-linkage of stereocilia in the guinea-pig labyrinth examined without the use of osmium as a fixative , 2004, Cell and Tissue Research.

[17]  S. Coombs,et al.  Modeling and measuring lateral line excitation patterns to changing dipole source locations , 2004, Journal of Comparative Physiology A.

[18]  Sheryl Coombs,et al.  Behavioral and neurophysiological assessment of lateral line sensitivity in the mottled sculpin, Cottus bairdi , 1990, Journal of Comparative Physiology A.

[19]  M G Evans,et al.  The actions of calcium on the mechano‐electrical transducer current of turtle hair cells. , 1991, The Journal of physiology.

[20]  S. Coombs,et al.  The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. , 2001, The Journal of experimental biology.

[21]  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.

[22]  R. Fay,et al.  What Is the Nature of Multisensory Interaction between Octavolateralis Sub-Systems? , 2002, Brain, Behavior and Evolution.

[23]  J. Gray,et al.  Some Observations on the Forces Acting on Neuromasts in Fish Lateral Line Canals , 1989 .

[24]  J F Webb,et al.  Gross morphology and evolution of the mechanoreceptive lateral-line system in teleost fishes. , 1989, Brain, behavior and evolution.

[25]  S Coombs,et al.  Form and function relationships in lateral line systems: comparative data from six species of Antarctic notothenioid fish. , 1994, Brain, behavior and evolution.

[26]  R. Fettiplace,et al.  The mechanical properties of ciliary bundles of turtle cochlear hair cells. , 1985, The Journal of physiology.

[27]  B. Kachar,et al.  High-resolution structure of hair-cell tip links. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Coombs,et al.  Diversity of Lateral Line Systems: Evolutionary and Functional Considerations , 1988 .

[29]  H. Bleckmann,et al.  Hydrodynamic stimuli and the fish lateral line , 2000, Nature.

[30]  J. Gray,et al.  The rigidity of fish and patterns of lateral line stimulation , 1982, Nature.

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

[32]  G. Geleoc,et al.  A quantitative comparison of mechanoelectrical transduction in vestibular and auditory hair cells of neonatal mice , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  A. Hudspeth,et al.  Putting ion channels to work: mechanoelectrical transduction, adaptation, and amplification by hair cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  H. Bleckmann,et al.  Lateral line reception in still- and running water , 2002, Journal of Comparative Physiology A.

[35]  J. Ashmore,et al.  Stiffness of sensory hair bundles in the sacculus of the frog , 1986, Hearing Research.

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

[37]  R. W. Murray.  The Lateralis Organs and their Innervation inXenopus laevis , 1955 .

[38]  Richard R. Fay,et al.  Hearing and Sound Communication in Fishes , 1981, Proceedings in Life Sciences.

[39]  A. Kroese,et al.  Frequency response of the lateral-line organ of xenopus laevis , 1978, Pflügers Archiv.

[40]  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.

[41]  J J Finneran,et al.  Hydrodynamic image formation by the peripheral lateral line system of the Lake Michigan mottled sculpin, Cottus bairdi. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[42]  J. Webb.  Mechanosensory Lateral Line: Microscopic Anatomy and Development , 2000 .

[43]  J. Pickles,et al.  Paired development of hair cells in neuromasts of the teleost lateral line , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  D. DeRosier,et al.  Actin in the inner ear: the remarkable structure of the stereocilium , 1980, Nature.

[45]  J. Gray,et al.  Mechanical Factors in the Excitation of the Lateral Lines of Fishes , 1988 .

[46]  D P Corey,et al.  Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[48]  J. Pickles,et al.  The organization of tip links and stereocilia on hair cells of bird and lizard basilar papillae , 1989, Hearing Research.

[49]  R. Goodyear,et al.  A Novel Antigen Sensitive to Calcium Chelation That is Associated with the Tip Links and Kinocilial Links of Sensory Hair Bundles , 2003, The Journal of Neuroscience.

[50]  A. Popper,et al.  The Evolutionary biology of hearing , 1992 .

[51]  J. Janssen,et al.  Non-visual feeding behavior of the mottled sculpin, Cottus bairdi, in Lake Michigan , 1985, Environmental Biology of Fishes.

[52]  S Coombs,et al.  Fibers innervating different parts of the lateral line system of an Antarctic notothenioid, Trematomus bernacchii, have similar frequency responses, despite large variation in the peripheral morphology. , 1992, Brain, behavior and evolution.

[53]  Barry L. Roberts,et al.  The Efferent System , 1989 .

[54]  Jelle Atema,et al.  Sensory Biology of Aquatic Animals , 1988, Springer New York.

[55]  J. O. Pickles.  A model for the mechanics of the stereociliar bundle on acousticolateral hair cells , 1993, Hearing Research.

[56]  A. M. Sutterlin,et al.  Possible Role of the Posterior Lateral Line in Obstacle Entrainment by Brook Trout (Salvelinus fontinalis) , 1975 .

[57]  H. Schlichting.  Boundary Layer Theory , 1955 .

[58]  Sheryl Coombs,et al.  Rheotaxis and prey detection in uniform currents by Lake Michigan mottled sculpin (Cottus bairdi) , 2003, Journal of Experimental Biology.

[59]  Sietse M. van Netten.  Hair cell mechano-transduction: Its influence on the gross mechanical characteristics of a hair cell sense organ , 1997 .

[60]  J. O. Pickles,et al.  Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction , 1984, Hearing Research.

[61]  A J Ricci,et al.  Mechanisms of Active Hair Bundle Motion in Auditory Hair Cells , 2002, The Journal of Neuroscience.

[62]  P. Gillespie,et al.  Regeneration of broken tip links and restoration of mechanical transduction in hair cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[64]  S M Khanna,et al.  Stiffness changes of the cupula associated with the mechanics of hair cells in the fish lateral line. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[66]  A. Flock,et al.  Sensory Transduction in Hair Cells , 1971 .

[67]  Peter G. Gillespie,et al.  Pulling springs to tune transduction: Adaptation by hair cells , 1994, Neuron.

[68]  Regulation of tension on hair-cell transduction channels: displacement and calcium dependence , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  Sietse M van Netten,et al.  Amiloride causes changes in the mechanical properties of hair cell bundles in the fish lateral line similar to those induced by dihydrostreptomycin , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  A. Flock,et al.  Stiffness of sensory-cell hair bundles in the isolated guinea pig cochlea , 1984, Hearing Research.

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

[72]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[73]  Gerard G. Harris,et al.  Evidence that the Lateral‐Line Organ Responds to Near‐Field Displacements of Sound Sources in Water , 1962 .

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

[75]  S Coombs,et al.  Physiological characterization of lateral line function in the Antarctic fish Trematomus bernacchii. , 1992, Brain, behavior and evolution.

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

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

[78]  Olav Sand,et al.  The Lateral Line and Sound Reception , 1981 .

[79]  A J Hudspeth,et al.  Gating-spring models of mechanoelectrical transduction by hair cells of the internal ear. , 1995, Annual review of biophysics and biomolecular structure.

[80]  K. Steel,et al.  Reduced climbing and increased slipping adaptation in cochlear hair cells of mice with Myo7a mutations , 2002, Nature Neuroscience.

[81]  G. Harris,et al.  Input-output characteristics of the lateral-line sense organs of Xenopus laevis. , 1965, The Journal of the Acoustical Society of America.

[82]  D P Corey,et al.  Analysis of the microphonic potential of the bullfrog's sacculus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[85]  S. Dijkgraaf.  THE FUNCTIONING and SIGNIFICANCE OF THE LATERAL‐LINE ORGANS , 1963, Biological reviews of the Cambridge Philosophical Society.

[86]  Morphological correlates of mechanotransduction in acousticolateral hair cells. , 1991, Scanning microscopy.

[87]  Peter Görner,et al.  Untersuchungen zur Morphologie und Elektrophysiologie des Seitenlinienorgans vom Krallenfrosch (Xenopus laevis Daudin) , 1963, Zeitschrift für vergleichende Physiologie.

[88]  Peter G. Gillespie,et al.  Cadherin 23 is a component of the tip link in hair-cell stereocilia , 2004, Nature.

[89]  S. M. van Netten.  Hydrodynamics of the excitation of the cupula in the fish canal , 1991 .

[90]  A J Hudspeth,et al.  Extracellular current flow and the site of transduction by vertebrate hair cells , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[91]  Stephan C. Schuster,et al.  Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells , 2004, Nature.

[92]  J. Gray,et al.  Acousticolateralis System in Clupeid Fishes , 1981 .

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

[94]  T. Pitcher,et al.  The sensory basis of fish schools: Relative roles of lateral line and vision , 1980, Journal of comparative physiology.

[95]  M Kössl,et al.  Nonlinear mechanical responses of mouse cochlear hair bundles , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[96]  G. Richardson,et al.  Mechano-electrical transducer currents in hair cells of the cultured neonatal mouse cochlea , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[97]  Kavita Shah,et al.  A Chemical-Genetic Strategy Implicates Myosin-1c in Adaptation by Hair Cells , 2002, Cell.

[98]  T. Dinklo,et al.  Signal processing by transducer channels in mammalian outer hair cells , 2003 .

[99]  Winfried Denk,et al.  Calcium imaging of single stereocilia in hair cells: Localization of transduction channels at both ends of tip links , 1995, Neuron.

[100]  Sietse M. van Netten,et al.  Gating energies and forces of the mammalian hair cell transducer channel and related hair bundle mechanics , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[101]  Sietse M van Netten,et al.  Channel gating forces govern accuracy of mechano-electrical transduction in hair cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[102]  Sietse M. van Netten,et al.  Temperature dependency of cupular mechanics and hair cell frequency selectivity in the fish canal lateral line organ , 2000, Journal of Comparative Physiology A.

[103]  R. Voigt,et al.  Responses of anterior lateral line afferent neurones to water flow. , 2000, The Journal of experimental biology.

[104]  A. Flock,et al.  Micromechanical properties of sensory hairs on receptor cells of the inner ear , 1983, Hearing Research.

[105]  R. Wubbels,et al.  AFFERENT RESPONSE OF A HEAD CANAL NEUROMAST OF THE RUFF (ACERINA-CERNUA) LATERAL LINE , 1992 .

[106]  D P Corey,et al.  Kinetics of the receptor current in bullfrog saccular hair cells , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.