Journal of Comparative Physiology A

, Volume 161, Issue 2, pp 295–304 | Cite as

Edge preference of retinal and tectal neurons in common toads (Bufo bufo) in response to worm-like moving stripes: the question of behaviorally relevant ‘position indicators’

  • H. J. Tsai
  • J. -P. Ewert
Article

Summary

Previous experiments have shown that during prey-catching behavior (orienting, snapping) in response to a worm-like moving stripe common toads.Bufo bufo (L.) exhibit a contrast-and direction-dependent edge preference. To a black (b) stripe moving against a white (w) background (b/w), they respond (R*) preferably toward the leading (l) rather the trailing (t) edge (Rl*> Rt*), thus displaying ‘head preference’. If the contrastdirection is reversed (w/b), the stripe's trailing edge is preferred (Rl*< Rt*), hence showing ‘tail preference’. In the present study, neuronal activities of retinal classes R2 and R3 and tectal classes T5(2) and T7 have been extracellularly recorded in response to leading and trailing edges of a 3 ° × 30 ° stripe simulating a worm and traversing the centers of their excitatory receptive fields (ERF) horizontally at a constant angular velocity in variable movement direction (temporo-nasal or naso-temporal).

The behavioral contrast-direction dependent edge preferences are best resembled by the responses (R) of prey-selective class T5(2) neurons (Rl∶ Rt=10∶1 for b/w, 0.3∶1 for w/b) and T7 neurons (Rl∶Rt=6∶1 for b/w, 0.4∶1 for w/b); the T7 responses may be dendritic spikes. This property can be traced back to off-responses dominated retinal class R3 neurons (Rl∶Rt=6∶1 for b/w, 0.5∶1 for w/b), but not to class R2 (Rl∶Rt =1.2∶1 for b/w and 0.9∶1 for w/b). The respective edge preference phenomena are independent of the direction of movement.

When stimuli were moved against a stationary black-white structured background, the ‘head preference’ to the black stripe and the ‘tail preference’ to the white stripe were maintained in class R3, T5(2), and T7 neurons. If the stripe traversed the ERF together with the structured background in the same direction at the same velocity, the responses of tectal class T5(2) and T7 neurons were strongly inhibited, particularly in the former. Responses of retinal R2 neurons in comparable situations could be reduced by about 50%, while class R3 neurons responded to both the stimulus and the moving background structure.

The results support the concept that the prey feature analyzing system in toads applies principles of (i) ‘parallel’ and (ii) ‘hierarchial’ information processing. These are (i) divergence of retinal R3 neuronal output contributes to stimulus edge positioning and (in combination with R2 output) area evaluation intectal neurons and to stimulus area evaluation and (in combination with R4 output) sensitivity for moving background structures inpre tectal neurons; (ii) convergence of tectal excitatory and pretectal inhibitory inputs specify the property of prey-selective tectal T5(2) neurons which are known to project to bulbar/spinal motor systems.

Abbreviations

ERF

excitatory receptive field

IRF

inhibitory receptive field

N

nasal

T

temporal

Rw

response to a worm-like stripe moving in the direction of its longer axis

RA

response to an antiworm-like stripe whose longer axis is oriented perpendicular to the direction of movement

Rl

response to the leading edge of a worm-like moving stripe

Rt

response to the trailing edge of a worm-like moving stripe

b/w

black stimulus against a white background

w/b

white stimulus against a black background

sm

structured moving background

ss

structured stationary background

u

minimal structure width of a structured background consisting of rectangular black and white patches in random distribution

HRP

horseradish peroxidase

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Apfelbach R, Wester U (1977) The quantitative effect of visual and tactile stimuli on the prey-catching behaviour of ferrets (Putorius furo L). Behav Processes 2:187–200Google Scholar
  2. Barlow HB (1953) Summation and inhibition in the frog's retina. J Physiol 119:69–88Google Scholar
  3. Barlow HB (1985) The twelfth Barlett Memoiral Lecture: The role of single neurons in the psychology of perception. Q J Exp Biol 37(A):121–145Google Scholar
  4. Burghagen H (1979) Der Einfluß von figuralen, visuellen Mustern auf das Beutefangverhalten verschiedener Anuren. Math-Nat dissertation, University of KasselGoogle Scholar
  5. Burghagen H, Ewert J-P (1982) Question of ‘head preference’ in response to worm-like dummies during prey-capture of toadsBufo bufo. Behav Processes 7:295–306Google Scholar
  6. Burghagen H, Ewert J-P (1983) Influence of the background for discriminating object motion from self-induced motion in toads (Bufo bufo L). J Comp Physiol 152:241–249Google Scholar
  7. Ewert J-P (1968) Der Einfluß von Zwischenhirndefekten auf die Visuomotorik im Beute- und Fluchtverhalten der Erdkröte (Bufo bufo L.). Z Vergl Physiol 61:41–70Google Scholar
  8. Ewert J-P (1974) The neural basis of visually guided behavior. Sci Am 230:34–42Google Scholar
  9. Ewert J-P (1984) Tectal mechanisms that underlie prey-catching and avoidance behaviors in toads. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum Press, New YorkGoogle Scholar
  10. Ewert J-P (1987) Neuroethology of releasing mechanisms: Prey-catching in toads. Behav Brain Sci (in press)Google Scholar
  11. Ewert J-P, Gebauer L (1973) Größenkonstanzphänomene im Beutefangverhalten der Erdkröte (Bufo bufo L.). J Comp Physiol 85:303–315Google Scholar
  12. Ewert J-P, Hock F (1972) Movement-sensitive neurones in the toad's retina. Exp Brain Res 16:41–59Google Scholar
  13. Ewert J-P, Institut für den Wissenschaftlichen Film (1982) Gestalt perception in the common toad I: Innate prey recognition. Inst Wiss Film C1430, GöttingenGoogle Scholar
  14. Ewert J-P, von Wietersheim A (1974a) Musterauswertung durch tectale and thalamus/praetectale Nervennetze im visuellen System der Kröte (Bufo bufo L.). J Comp Physiol 92:131–148Google Scholar
  15. Ewert J-P, Wietersheim A von (1974b) Der Einfluß von Thalamus/Praetectum-Defekten auf die Antwort von Tectum-Neuronen gegenüber bewegten visuellen Mustern bei der Kröte (Bufo bufo L.). J Comp Physiol 92:149–160Google Scholar
  16. Ewert J-P, Speckhardt I, Amelang W (1970) Visuelle Inhibition und Exzitation im Beutefangverhalten der Erdkröte (Bufo bufo L.). Z Vergl Physiol 68:84–110Google Scholar
  17. Goethe F (1940) Beiträge zur Biologie des Iltis. Z Säugetierkunde 15:180–221Google Scholar
  18. Grüsser O-J, Grüsser-Cornehls U (1968) Neurophysiologische Grundlagen visueller angeborener Auslösemechanismen beim Frosch. Z Vergl Physiol 59:1–24Google Scholar
  19. Grüsser O-J, Grüsser-Cornehls U (1976) Neurophysiology of the anuran visual system. In: Llinás R, Precht W (eds) Frog Neurobiology. Springer, Berlin Heidelberg New YorkGoogle Scholar
  20. Grüsser-Cornehls U (1984) The neurophysiology of the amphibian optic tectum. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum Press, New YorkGoogle Scholar
  21. Hartline HK (1940) The receptive fields of optic nerve fibers. Am J Physiol 130:690–699Google Scholar
  22. Herbst G (1981) Quantitative Untersuchungen zur Frage der Invariantenbildung beim Beuteerkennen verschiedener Subspecies der Erdkröte (Bufo bufo bufo undBufo bufo spinosus). Staatsexamen Thesis, University of KasselGoogle Scholar
  23. Ingle D (1968) Visual releasers of prey catching behavior in frogs and toads. Brain Behav Evol 1:500–518Google Scholar
  24. Ingle D (1983) Brain mechanisms of visual localization by frogs and toads. In: Ewert J-P, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New YorkGoogle Scholar
  25. Ingle D, McKinley D (1978) Effects of stimulus configuration on elicited prey catching by the marine toad (Bufo marinus). Anim Behav 26:885–891Google Scholar
  26. Ingle DJ, Quinn S (1982) Retrograde labelling of neurons of known behavioral function in frog tectum. Soc Neurosci Abstr 8:406Google Scholar
  27. Julesz B (1976) Experiments in the visual perception of texture. In: Held R, Richards W (eds) Recent progress in perception (Readings from Scientific American). Freeman, San FranciscoGoogle Scholar
  28. Lettvin JY, Maturana HR, McCulloch WS, Pitts WH (1959) What the frog's eye tells the frog's brain. Proc Inst Radio Eng NY 47:1940–1951Google Scholar
  29. Leyhausen P (1965) Über die Funktion der relativen Stimmungshierarchie (dargestellt am Beispiel der phylogenetischen und ontogenetischen Entwicklung des Beutefangs von Raubtieren). Z Tierpsychol 22:412–494Google Scholar
  30. Matsumoto N, Schwippert WW, Ewert J-P (1986) Intracellular activity of morphologically identified neurons of the grass frog's optic tectum in response to moving configurational visual stimuli. J Comp Physiol A 159:721–739Google Scholar
  31. Maturana HR, Lettvin JY, McCulloch WS, Pitts WH (1960) Anatomy and physiology of vision in the frog (Rana pipiens). J Gen Physiol 43:129–176Google Scholar
  32. Rasa OA (1973) Prey capture, feeding techniques, and their ontogeny in the African dwarf mongoose (Helogale undulata rufula. Z Tierpsychol 32:449–488Google Scholar
  33. Satou M, Ewert J-P (1985) The antidromic activation of tectal neurons by electrical stimuli applied to the caudal medulla oblongata in the toadBufo bufo L. J Comp Physiol A 157:739–748Google Scholar
  34. Székely G, Lázár G (1976) Cellular and synaptic architecture of the optic tectum. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 407–434Google Scholar
  35. Tsai HJ, Ewert J-P (1987) Influence of stationary and moving background structures on the response of visual neurons to moving configurational stimuli in toads. Brain Behav Evol (in press)Google Scholar
  36. Tsai HJ, Burghagen H, Schürg-Pfeiffer E, Ewert J-P (1983) Neuronal correlates of edge-orientation in toadsBufo bufo. Naturwissenschaften 70:310–311Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • H. J. Tsai
    • 1
  • J. -P. Ewert
    • 1
  1. 1.Abteilung NeuroethologieFB 19 der Universität KasselKasselGermany

Personalised recommendations