Lateral line stimulation patterns and prey orienting behavior in the Lake Michigan mottled sculpin (Cottus bairdi)

Information contained in the spatial excitation pattern along arrayed sensors in the lateral line system of Lake Michigan mottled sculpin, as well as other surface-feeding fish and amphibians, is thought to play a fundamental role in guiding prey-orienting behaviors. However, the way in which prey location is encoded by the excitation pattern and used by the nervous system to direct orienting behaviors is largely unknown. In this study, we test the hypothesis that mottled sculpin use excitation peaks (local ‘hot spots’) to determine the somatotopic location of an artificial prey (vibrating sphere/dipole source) along the body surface. Dipole orientation (axis of sphere vibration re: long axis of the fish) is manipulated to produce excitatory peaks in different body locations without changing the actual sphere location. Our results show that orienting accuracy is largely independent of source orientation, but not source distance and that turning directions are not guided by local hot spots in the somatotopic activation pattern of the lateral line.

[1]  P. Grobstein,et al.  The organization of descending tectofugal pathways underlying orienting in the frog, Rana pipiens , 2004, Experimental Brain Research.

[2]  E I Knudsen,et al.  A neural map of auditory space in the owl. , 1978, Science.

[3]  R. Northcutt,et al.  The primary projections of the lateral-line nerves of the Florida gar, Lepisosteus platyrhincus. , 1991, Brain, behavior and evolution.

[4]  Sensorimotor function of the midbrain tectum. I. Introduction. What is the optic tectum? , 1975, Neurosciences Research Program bulletin.

[5]  E. Knudsen Auditory and visual maps of space in the optic tectum of the owl , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  E. Vandenbussche,et al.  Convergence of retinal and lateral line stimulation on tectum opticum and cerebellar neurones. , 1967, Archives internationales de physiologie et de biochimie.

[7]  H. Vanegas,et al.  Comparative neurology of the optic tectum , 1984 .

[8]  J. Ewert Neural mechanisms of prey-catching and avoidance behavior in the toad (Bufo bufo L.). , 1970, Brain, behavior and evolution.

[9]  P. Grobstein,et al.  The organization of descending tectofugal pathways underlying orienting in the frog, Rana pipiens , 2004, Experimental Brain Research.

[10]  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.

[11]  J. Ewert Tectal Mechanisms That Underlie Prey-Catching and Avoidance Behaviors in Toads , 1984 .

[12]  R. Fay,et al.  Bimodal units in the torus semicircularis of the toadfish (Opsanus tau). , 2001, The Biological Bulletin.

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

[14]  P. Morse Vibration and Sound , 1949, Nature.

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

[16]  Simon Haykin,et al.  Neural Networks: A Comprehensive Foundation , 1998 .

[17]  B. Claas,et al.  Analysis of surface wave direction by the lateral line system of Xenopus: Source localization before and after inactivation of different parts of the lateral line , 1996, Journal of Comparative Physiology A.

[18]  C. Bell Central distribution of octavolateral afferents and efferents in a teleost (mormyridae) , 1981, The Journal of comparative neurology.

[19]  H. Karten,et al.  Differential projections of ordinary lateral line receptors and electroreceptors in the gymnotid fish, Apteronotus (Sternarchus) albifrons , 1974, The Journal of comparative neurology.

[20]  Sheryl Coombs,et al.  Dipole source localization by the mottled sculpin II. The role of lateral line excitation patterns , 1997, Journal of Comparative Physiology A.

[21]  Sheryl Coombs,et al.  Signal detection theory, lateral-line excitation patterns and prey capture behaviour of mottled sculpin , 1999, Animal Behaviour.

[22]  B. Claas,et al.  Directional sensitivity of lateral line units in the clawed toadXenopus laevis Daudin , 1986, Journal of Comparative Physiology A.

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

[24]  J. Nazuno Haykin, Simon. Neural networks: A comprehensive foundation, Prentice Hall, Inc. Segunda Edición, 1999 , 2000 .

[25]  B. Stein,et al.  Multimodal Representation in the Superior Colliculus and Optic Tectum , 1984 .

[26]  E. Knudsen,et al.  Creating a unified representation of visual and auditory space in the brain. , 1995, Annual review of neuroscience.

[27]  Julie Goulet,et al.  Object localization through the lateral line system of fish: theory and experiment , 2007, Journal of Comparative Physiology A.

[28]  J. Delgado-García,et al.  Information processing underlying gaze control , 1994 .

[29]  Sietse M van Netten,et al.  Source location encoding in the fish lateral line canal , 2006, Journal of Experimental Biology.

[30]  B. Stein,et al.  The Merging of the Senses , 1993 .

[31]  J. H. L. M. Goossens,et al.  Mapping of sound direction in the trout lower midbrain , 1995, Neuroscience Letters.

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

[33]  B. Torres,et al.  9 – On the Role of Goldfish Optic Tectum in the Generation of Eye Movements , 1994 .

[34]  S. Coombs Natural Orienting Behaviors For Measuring Lateral Line Function , 1995 .

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

[36]  Horst Bleckmann,et al.  Prey Identification and Prey Localization in Surface-feeding Fish and Fishing Spiders , 1988 .

[37]  Sheryl Coombs,et al.  Dipole source localization by mottled sculpin. I. Approach strategies , 1997, Journal of Comparative Physiology A.

[38]  Nico A. M. Schellart Interrelations Between the Auditory, the Visual and the Lateral Line Systems of Teleosts; a Mini-Review of Modelling Sensory Capabilities , 1991 .

[39]  C. A. Mccormick Central connection of the octavolateralis nerves in the pike cichlid, Crenicichla lepidota , 1983, Brain Research.

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

[41]  G. Meredith Peripheral configuration and central projections of the lateral line system in Astronotus ocellatus (cichlidae): A nonelectroreceptive teleost , 1984, The Journal of comparative neurology.

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

[43]  R. Leonard,et al.  The octavolateral systems in the stingray, Dasyatis sabina. I. Primary projections of the octaval and lateral line nerves , 1993, The Journal of comparative neurology.

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

[45]  Direction Coding in Central Parts of the Lateral Line System , 1989 .

[46]  D. Bodznick,et al.  Elasmobranch vision: multimodal integration in the brain. , 1990, The Journal of experimental zoology. Supplement : published under auspices of the American Society of Zoologists and the Division of Comparative Physiology and Biochemistry.

[47]  George Cybenko,et al.  Approximation by superpositions of a sigmoidal function , 1989, Math. Control. Signals Syst..

[48]  N. Schellart,et al.  Interrelationship of Acousticolateral and Visual Systems in the Teleost Midbrain , 1989 .

[49]  S. Coombs,et al.  The overlapping roles of the inner ear and lateral line: the active space of dipole source detection. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  C. Comer,et al.  Visually elicited turning behavior in Rana pipiens: comparative organization and neural control of escape and prey capture , 1996, Journal of Comparative Physiology A.

[51]  B. Torres,et al.  Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish , 1998, Experimental Brain Research.

[52]  Wolf Hanke,et al.  A hydrodynamic topographic map in the midbrain of goldfish Carassius auratus , 2003, Journal of Experimental Biology.

[53]  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.

[54]  Peripheral Processing by the Lateral Line System of the Mottled Sculpin ( Cottus bairdi ) , 1989 .

[55]  T. Finger,et al.  Central organization of eighth nerve and mechanosensory lateral line systems in the brainstem of ictalurid catfish , 1984, The Journal of comparative neurology.

[56]  M. Kamermans,et al.  An electrophysiological study of the topographical organization of the multisensory torus semicircularis of the rainbow trout , 1987 .

[57]  Georg M. Klump,et al.  Methods in Comparative Psychoacoustics , 1995, BioMethods.

[58]  S. Coombs,et al.  Dipole source localization by mottled sculpin. III. Orientation after site-specific, unilateral denervation of the lateral line system , 1998, Journal of Comparative Physiology A.

[59]  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.

[60]  James L. McClelland,et al.  Parallel distributed processing: explorations in the microstructure of cognition, vol. 1: foundations , 1986 .

[61]  J. Mogdans,et al.  Transformation of peripheral inputs by the first-order lateral line brainstem nucleus , 1998, Journal of Comparative Physiology A.

[62]  P. Grobstein,et al.  Neuronal organization underlying visually elicited prey orienting in the frog—I. Effects of various unilateral lesions , 1987, Neuroscience.

[63]  Sheryl Coombs,et al.  Information-processing demands in electrosensory and mechanosensory lateral line systems , 2002, Journal of Physiology-Paris.

[64]  P. Görner,et al.  The area octavo-lateralis in Xenopus laevis , 2004, Cell and Tissue Research.

[65]  N. Schellart Acousticolateral and visual processing and their interaction in the torus semicircularis of the trout, Salmo gairdneri , 1983, Neuroscience Letters.

[66]  R. Fay,et al.  Hot-film anemometry for measuring lateral line stimuli. , 1989, The Journal of the Acoustical Society of America.

[67]  E I Knudsen,et al.  Computational maps in the brain. , 1987, Annual review of neuroscience.

[68]  J. New,et al.  Central topography of anterior lateral line nerve projections in the channel catfish, Ictalurus punctatus. , 1994, Brain, behavior and evolution.

[69]  R L Puzdrowski,et al.  Peripheral distribution and central projections of the lateral-line nerves in goldfish, Carassius auratus. , 1989, Brain, behavior and evolution.

[70]  S. Coombs,et al.  Nearfield detection of dipole sources by the goldfish (Carassius auratus) and the mottled sculpin (Cottus bairdi). , 1994, The Journal of experimental biology.

[71]  M S Loop,et al.  Merging of modalities in the optic tectum: infrared and visual integration in rattlesnakes. , 1978, Science.

[72]  D. Sparks Neural cartography: sensory and motor maps in the superior colliculus. , 1988, Brain, behavior and evolution.

[73]  Teuvo Kohonen,et al.  Self-organization and associative memory: 3rd edition , 1989 .

[74]  Stanton A. Glantz,et al.  Primer of biostatistics : statistical software program version 6.0 , 1981 .

[75]  D. Varjú,et al.  Localization and Orientation in Biology and Engineering , 1984, Proceedings in Life Sciences.

[76]  D. M. Guthrie,et al.  Motor responses to localized electrical stimulation of the tectum in the freshwater perch (perca fluviatilis) , 1986, Neuroscience.

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

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

[79]  S. Coombs,et al.  Mechanosensory‐based orientation to elevated prey by a benthic fish , 2000 .

[80]  Peter Görner,et al.  Lateral-Line Input and Stimulus Localization in the African Clawed Toad Xenopus SP , 1984 .