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Prey-capture in the African clawed toad (Xenopus laevis): comparison of turning to visual and lateral line stimuli

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Abstract

Separately delivered visual and lateral line stimuli elicit similar but not identical orientation and approach by intact, sighted Xenopus. Response frequencies for visual stimuli declined sharply for distant or caudal stimuli while those for lateral line stimuli changed little. Turn angles correlated highly with stimulus angles but were smaller on average, so regression slopes were less than one. Regression slopes were smaller for visual than for lateral line stimuli, but this apparent difference was due to different distributions of stimulus distance interacting with the toad’s rotation center. Errors in final headings, most often under-rotations, did not differ by modality. Frequencies of lunges and arm capture movements were higher for visual stimuli both overall and especially for rostral proximal stimuli. The results demonstrate accurate orientation by sighted Xenopus to visual and lateral line stimuli; they are consistent with expectations based on in-register tectal maps. Orientation to lateral line stimuli is similar to previous results with blinded animals, revealing no heightened acuity in the latter. Modality differences indicate that the lateral line system is better for omnidirectional orientation and approach to distant stimuli whereas the visual system is more attuned to nearby rostral stimuli and more apt to mediate strikes.

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References

  • Braun CB, Coombs S, Fay RR (2002) What is the nature of multisensory interaction between octavolateralis subsystems? Brain Behav Evol 59:162–176

    Article  PubMed  Google Scholar 

  • Claas B (1994) Removal of eyes in early larval stages alters the responses of the clawed toad, Xenopus laevis, to surface waves. Physiol Behav 56:423–428

    Article  PubMed  CAS  Google Scholar 

  • Claas B, Münz H (1996) 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. J Comp Physiol A 178:253–268

    Article  PubMed  CAS  Google Scholar 

  • Claas B, Münz H, Görner P (1993) Reaction to surface waves by Xenopus laevis Daudin: are sensory systems other than the lateral line involved? J Comp Physiol A 172:759–765

    Article  PubMed  CAS  Google Scholar 

  • Coombs S, New JG (2002) Preface: multimodal sensory guidance of complex behaviors. Brain Behav Evol 59:159–161

    Article  Google Scholar 

  • Dusenbury DB (1992) Sensory ecology: how animals acquire and respond to information. WH Freeman, New York

    Google Scholar 

  • Elepfandt A (1982) Accuracy of taxis response to water-waves in the clawed toad (Xenopus laevis Daudin) with intact or with lesioned lateral line system. J Comp Physiol 148:535–545

    Article  Google Scholar 

  • Elepfandt A (1984) The role of ventral lateral line organs in water-wave localization in the clawed toad (Xenopus laevis). J Comp Physiol 154:773–780

    Article  Google Scholar 

  • Elepfandt A (1989) Wave analysis by amphibians. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, Berlin Heidelberg New York, pp. 527–541

    Google Scholar 

  • Elepfandt A, Wiedemer L (1987) Lateral-line responses to water-surface waves in the clawed frog, Xenopus laevis. J Comp Physiol A 160:667–682

    Article  Google Scholar 

  • Ewert J-P (1984) Tectal mechanisms that underlie prey-catching and avoidance behaviors in toads. In: Vanegas H (ed) The comparative neurology of the optic tectum. Plenum, New York, pp. 247–416

    Google Scholar 

  • Ewert J-P (1997) Neural correlates of key stimulus and releasing mechanism: a case study and two concepts. Trends Neurosci 20:332–339

    Article  PubMed  CAS  Google Scholar 

  • Favilla M, Henning W, Ghez C (1989) Trajectory control in targeted force impulses. VI. Independent specification of response amplitude and direction. Exp Brain Res 75:280–294

    Article  PubMed  CAS  Google Scholar 

  • Gaze RM, Keating MJ, Szekely G, Beazley L (1970) Binocular interaction in the formation of specific intertectal neuronal connections. Proc R Soc Lond B Biol Sci 175:107–147

    Article  PubMed  CAS  Google Scholar 

  • Gaze RM, Keating MJ, Chung SH (1974) The evolution of the retinotectal map during development in Xenopus. Proc R Soc Lond B Biol Sci 185:301–330

    PubMed  CAS  Google Scholar 

  • Görner P (1973) The importance of the lateral line system for the perception of surface waves in the claw toad, Xenopus laevis, Daudin. Experientia 29:295–296

    Article  Google Scholar 

  • Görner P (1976) Source localization with labyrinth and lateral line in the clawed toad (Xenopus laevis). In: Schuijf A, Hawkins AD (eds) Sound reception in fish. Elsevier, Amsterdam, pp. 171–184

    Google Scholar 

  • Görner P, Moller P, Weber W (1984) Lateral-line input and stimulus localization in the African clawed toad Xenopus sp. J Exp Biol 108:315–328

    Google Scholar 

  • Gregory RL (1966) Auge und Gehirn: Zur Psychophysiologie des Sehens. Kindler Verlag, München

    Google Scholar 

  • Grobstein P (1988) Between retinotectal projection and directed movement: topography of a sensorimotor interface. Brain Behav Evol 31:34–48

    PubMed  CAS  Google Scholar 

  • Grüsser-Cornehls U (1984) The neurophysiology of the amphibian optic tectum. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum, New York, pp. 211–245

    Google Scholar 

  • Grüsser O-J, Grüsser-Cornehls U (1976) Neurophysiology of the anuran visual system. In: Llinas R, Precht W (eds) Frog neurobiology: a handbook. Springer, Berlin Heidelberg New York, pp. 297–385

    Google Scholar 

  • Heiligenberg W (1991) Neural nets in electric fish. MIT, Cambridge

    Google Scholar 

  • Ingle DJ (1976) Behavioral correlates of central visual function in anurans. In: Llinas R, Precht W (eds) Frog neurobiology: a handbook. Springer, Berlin Heidelberg New York, pp. 435–451

    Google Scholar 

  • Jacobson M (1962) The representation of the retina on the optic tectum of the frog. Correlation between retinotectal magnification factor and retinal ganglion cell count. Q J Exp Physiol 47:170–178

    CAS  Google Scholar 

  • King AJ (1999) Sensory experience and the formation of a computational map of auditory space in the brain. Bioessays 21:900–911

    Article  PubMed  CAS  Google Scholar 

  • King AJ, Parsons CH (1999) Improved auditory spatial acuity in visually deprived ferrets. Eur J Neurosci 11:3945–3956

    Article  PubMed  CAS  Google Scholar 

  • Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2:1177–1194

    PubMed  CAS  Google Scholar 

  • Knudsen EI (2002) Instructed learning in the auditory localization pathway of the barn owl. Nature (London) 417:322–328

    Article  CAS  Google Scholar 

  • Knudsen EI, Knudsen PF (1989) Visuomotor adaptation to displacing prisms by adult and baby barn owls. J Neurosci 9:3297–3305

    PubMed  CAS  Google Scholar 

  • Knudsen EI, Blasdel GG, Konishi M (1979) Sound localization by the barn owl measured with the search coil technique. J Comp Physiol 133:1–11

    Article  Google Scholar 

  • Knudsen EI, Esterly SD, Knudsen PF (1984) Monaural occlusion alters sound localization during a sensitive period in the barn owl. J Neurosci 4:1001–1011

    PubMed  CAS  Google Scholar 

  • Kramer G (1933) Untersuchungen uber die Sinnesleistungen und das Orientierungsverhalten von Xenopus laevis Daud. Zool Jb Physiol 52:629–676

    Google Scholar 

  • du Lac S, Knudsen EI (1990) Neural maps of head movement vector and speed in the optic tectum of the barn owl. J Neurophysiol 63:131–146

    PubMed  CAS  Google Scholar 

  • Lindquist SB, Bachmann MD (1982) The role of visual and olfactory cues in the prey catching behavior of the tiger salamander Ambystoma tigrinum. Copeia 1982:81–90

    Article  Google Scholar 

  • Lowe DA (1986) Organization of lateral line and auditory areas in the midbrain of Xenopus laevis. J Comp Neurol 245:498–513

    Article  PubMed  CAS  Google Scholar 

  • Mogdans J, Barenbrock J, Bleckmann H (2002) Sighted topminnows, Aplocheilus lineatus, use the lateral line for surface wave discrimination. Copeia 2002:190–194

    Article  Google Scholar 

  • Montgomery JC, Macdonald F, Baker CF, Carton AG (2002) Hydrodynamic contributions to multimodal guidance of prey capture behavior in fish. Brain Behav Evol 59:190–198

    Article  PubMed  Google Scholar 

  • New JG (2002) Multimodal integration in the feeding behaviors of predatory teleost fish. Brain Behav Evol 59:177–189

    Article  PubMed  Google Scholar 

  • Rudolph P (1967) Zum Ortungsverhalten von Gyrinus substraticus Steph (Taumelkäfer). Z Vergl Physiol 50:341–361

    Article  Google Scholar 

  • Schürg-Pfeiffer E, Spreckelsen C, Ewert J-P (1993) Temporal discharge patterns of tectal and medullary neurons chronically recorded during snapping toward prey in toads Bufo bufo spinosus. J Comp Physiol A 173:363–376

    Article  Google Scholar 

  • Stein BE, Meredith MA (1993) The merging of the senses. MIT, Cambridge

    Google Scholar 

  • Stull AK, Gruberg ER (1998) Prey selection in the leopard frog: choosing in biased and unbiased situations. Brain Behav Evol 52:37–45

    Article  PubMed  CAS  Google Scholar 

  • Traub B, Elepfandt A (1990) Sensory neglect in a frog: evidence of early evolution of attentional processes in vertebrates. Brain Res 520:105–107

    Article  Google Scholar 

  • Udin SB (1990) Plasticity in the ipsilateral visuotectal projection persists after lesions of one nucleus isthmi in Xenopus. Exp Brain Res 79:338–344

    Article  PubMed  CAS  Google Scholar 

  • Udin SB, Keating MJ (1981) Plasticity in a central nervous pathway in Xenopus: anatomical changes in the isthmo-tectal projection after larval eye rotation. J Comp Neurol 203:575–594

    Article  PubMed  CAS  Google Scholar 

  • Valentine DE, Sinha SR, Moss CF (2002) Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus. J Comp Physiol A 188:89–108

    Article  Google Scholar 

  • Zittlau KE, Claas B, Münz H (1986) Directional sensitivity of lateral line units in the clawed toad Xenopus laevis Daudin. J Comp Physiol A 158:469–477

    Article  Google Scholar 

Download references

Acknowledgment

Volker Duerr (University of Bielefeld) generously provided a Delphi program that was modified for the video frame analysis. These experiments were performed in accord with the NAS Guide for the Care and Use of Laboratory Animals and approved by the CSU IACUC.

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Correspondence to Jeffrey Dean.

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Claas, B., Dean, J. Prey-capture in the African clawed toad (Xenopus laevis): comparison of turning to visual and lateral line stimuli. J Comp Physiol A 192, 1021–1036 (2006). https://doi.org/10.1007/s00359-006-0137-2

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  • DOI: https://doi.org/10.1007/s00359-006-0137-2

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