J. comp. Physiol. 128, 189-192 (1978) Journal of Comparative Physiology. A �9 by Springer-Verlag 1978

Key Stimuli of Prey for Toads (Bufo bufo L.): Configuration and Movement Patterns *

H.-W. Borchers, H. Burghagen, and J.-P. Ewert

Neuroethology and Biocybernetic Laboratories, University of Kassel, D-3500 Kassel, Federal Republic of Germany

Accepted August 22, 1978

Summary. The abil i ty of the C o m m o n Toad Bufo bufo (L.) to dist inguish between a worm-like and an ant iworm-l ike (e.g., a bar at right angles to its direc- t ion of mot ion) moving stripe is no t generally altered by movemen t dynamics, such as velocity of mot ion or by par t icular movemen t p a t t e r n s - s o far as has been investigated. A small square stimulus, however, with its " i nd i f f e r en t " shape is more attractive as prey for the toad when displaced in a stepwise manner , rather t han moved at cor responding con t inuous (con- stant) velocity. Step frequencies of 1 to 2 cps were found to have opt imal releasing values.

Introduction

Toads Bufo bufo (L.) dist inguish visual prey objects f rom predators or behavioral ly irrelevant objects on the basis of conf igura t ional s t imulus parameters l inked with the direct ion of s t imulus movemen t (for review see Ewert, 1976). Our previous experiments have been per formed with stimuli moved cont in- uously at cons tan t velocities. Consider ing the richness of movemen t pat terns of the na tu ra l prey objects, however, our experimental s t imulus movements seem to represent only a crude simplification. Sensitivity to je rky movements was recently observed in the vi- sually guided prey-catching behavior of sa lamanders (Roth, 1978). The present study with C o m m o n Toads Bufo bufo (L.) investigates the influence of movement dynamics on the d iscr iminat ion of moving configura- t ional stimuli.

Method

Stimulus Configurations

The standard stimuli are shown in Fig. 2A-C: A black 3 x 30 mm 2 stripe moved in a worm-like way with its long axis parallel to

* Supported by the Deutsche Forschungsgemeinschaft Ew 7/6

the horizontal direction of motion (A), a black 3 x 30 mm z stripe moved antiworm-like with its axis perpendicular to the direction of motion (B), and a black 6 x 6 mm 2 square (C). All stimuli were moved on a white background at a distance of 7 cm from the toad's eyes. The amount of the stimulus background contrast was C=(Lb-Ls) / (L b +L~) =0.9, with L [cd x m -z] luminances of the stimulus (s) and the background (b).

Movement Patterns

The stimulus was moved linearly in a horizontal (x-) direction by a motor-driven belt system (Fig. 1). Movement patterns-so- called step movements-were generated by different waveform functions (Fig. 2a-c): Square wave (a), triangular (b) or sinusoidal (c). The pulses of the waveforms controlled the velocity of the belt-motor (Fig. 1). The amplitudes of the pulses corresponded to the stimulus movement velocity, vm; the baseline level of the pulses was zero (Fig. 2 above). The maximum peak-to-peak level was the same in all cases (Fig. 2a-c) and it corresponded to a stimulus movement velocity (Vm) of 18 mm/s. Thus stimuli could be moved in steps by 3 different modes (see lower traces in Fig. 2a-c).

Fig. 1. Experimental procedure for measurements of the toad's (Bufo bufo) prey-catching activity in response to a black stimulus object (s) moved in horizontal (x-) direction from left to right on a white belt (b). The belt is driven continuously by an electronic device consisting of an electric motor (M), a tachogenerator (TG) and a controller (C). Step-movements can be generated by means of a function generator (FG) which gives the reference input for the controller

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Fig. 2. Influence of stimulus objects of different configurations (A-C) moved in stepwise manner by different step frequencies and functions (a-c) on the prey-catching orienting activity of the toad Bufo bufo. Each curve point represents average response activities from 20 different animals. Upper traces: Reference input of the controller (see Fig. 1). Lower traces: Output voltage of the tachogenerator as an index of the movement velocity v~, of the stimulus. (The ripple in the records is part of the pulsating DC voltage of the tachogenerator. Distortions at 100 cps may be neglected in the present experiments because the toad's visual system is unable to resolve these frequency patterns). Records above: Step movement frequencies of 2 cps; records below: Step movement frequencies of 5 cps

H.-W. Borchers et al. : Configuration and Movement Patterns 191

Within each waveform (a, b, or c) the frequency F was varied in the range 0.2 _< F< 100 (cps). Variation of the pulse (step) frequency did not change the stimulus displacement time in am: The average step movement velocity was constant at v~=9 mm/s in all cases.

Movement Dynamics (Fig. 2a-c)

At constant frequency, in (a) the stimulus velocity within a half cycle remained constant, in (b) the velocity within a half cycle varied with constant acceleration, and in (c) the acceleration within the cycle varied cosinusoidally. By increasing the frequency in (a) the stimulus velocity within a half cycle remained constant, in (b) the amount of the acceleration increased and in (c) the change of the acceleration increased.

Measure of the Releasing Value of the Stimulus

During the experiment the toad sat within a cylindrical glass vessel in front of the belt system (Fig. 1). If the stimulus fitted the category prey the toad responded with orienting movements of the head and body toward the stimulus object. The number of prey-catching orienting movements per traverse of the stimulus through a frontal part of the binocular visual field of 104 ~ visual angle (M80 mm, and a time interval of 20 s) was taken as a measure of the releasing value of the stimulus as a prey object.

Experiments were performed with a total of 20 toads. The influence of movement functions was tested in three groups (Fig. 2a-c) being separated by 24 h recovery periods. Within each group the frequency of the waveform functions was changed succes- sively in random order.

The prey-catching activity in response to the square (Fig. 2 C, a-c) averaged less than was obtained for the worm-like object. Surprisingly, here the prey- catching activity showed a statistically significant de- pendence on the step-movement frequency. For a l l three movement modes (a-c), step frequencies of 1-2 cps were found to be optimal releasers (p<0.01; t-test). Step-movements of 100 cps had the same weak releasing value as stimuli moved continuously at 9 mm/s. These step frequencies cannot be resolved by the visual system of the toad. The value is far above threshold of the fusion frequency (Ewert, 1968; Grfisser-Cornehls, 1968).

Further experiments with the square object were carried out to answer the question of whether the time- pattern or the particular spatial displacement pattern of the stimulus was the significant feature. The results showed that in the investigated velocity range 4.5_-<vm<36 mm/s of square wave pulse-generated step movement patterns the optimal frequency of 1-2 cps did not alter in the higher or lower ranges by a statistically significant amount. This indicates that the time pattern rather than the spatial displace- ment pattern of the steps is the important stimulus feature.

Discussion

Results

Responses to the worm-like object are shown in Fig. 2A, a~c. The average prey-catching activity of the toads was increased slightly when square (a), triangle (b) or sinusoidal generated step movements had frequencies in the range of 1-2 cps. The response activity to the ant iworm (Fig. 2B, a-c) was zero for all movement modes and step frequencies tested.

In evaluating the results shown in Fig. 2A a possi- b l e " saturation effect" should be considered: because the worm-like configuration is such a strong prey stimulus for the toad it is not possible to increase the catching activity any further. Therefore compara- tive experiments with a worm stimulus of same size but weak contrast (Cg0 .5 ) were carried out. In this case the level of prey-catching activity was decreased, but the effects of step movements showed no remark- able difference f rom the previous results.

In another set of experiments the worm and anti- worm stimuli were moved at constant (continuous) velocity vm=4.5, 9, 18 or 36 mm/s. The toads showed a clear preference for the worm configuration. The probabili ty that the toads made a "misinterpre- t i o n " - t r a c k i n g an a n t i w o r m - i n the present selec- tion test at all movement velocities investigated was p < 0.01 (t-test).

The results show that the ability of the toad Bufo bufo to distinguish worm-like f rom antiworm-like ob- jects is not altered by the dynamics of the s t i m u l u s - angular velocity and displacement pattern so far as has been investigated. In case of an "indifferent prey st imulus" configuration, such as with a square, the movement pattern may have strong effects on the releasing value. Thus, prey selection by the toad Bufo bufo may depend on both configuration and move- ment pattern. J.Y. Lettvin writes: " f rogs will leap to capture any object the size of an insect or worm, providing it moves like one" (Lettvin et al., 1959). Ewert and Kallweidt (in preparation) recently found in the frog Rana temporaria (L.) that particular move- ment patterns of a visual contrast stimulus, such as step movements (1 step/s), are important features for a stimulus to be categorized as prey. Similar results were obtained by D. Ingle (personal communication, 1977). Roth, recently working in our laboratory, observed also an influence of jerky movements on the prey catching activity in salamanders Hydro- mantes genei (Roth, 1978). The movement patterns investigated in all these studies, however, are presum- ably only a part of a whole complex. In our future research the movement dynamics of natural prey ob- jects must be analyzed and possibly compared with the optimal step frequencies of 1-2 cps obtained in

192 H.-W. Borchers et al. : Configuration and Movement Patterns

the presen t s tudy (Borchers et al., in p r epa ra t i on , 1978). I t is in teres t ing to no te tha t square prey dummies mov ing by steps in tha t range were also p re fe r red by Hydromantes genei (Roth , 1978).

The ques t ion o f neu rona l systems sensit ive to par- t icular k inds o f m o v e m e n t dynamics has been men- t i oned bu t has no t yet been ana lyzed quant i ta t ive ly . Grf isser et al. (1968) r e p o r t e d for the f rog Rana escu- lenta t ha t the exponen t o f the s t imulus veloci ty power func t ion was no t a l te red in re t ina l R 2 neurons , if the s t imulus was m o v e d in steps t h r o u g h the recept ive field. The response o f pa r t i cu l a r neurons of the t o a d ' s (Bufo bufo) opt ic t ec tum seemed to be ex t remely sensi- t ive to cer ta in m o v e m e n t dynamics o f a visual s t im- ulus (Ewert et al., in p repara t ion) . F o r example , a 5 ~ x 5 ~ square m o v e d m a n u a l l y t h r o u g h the center of the recept ive field ac t iva ted the neu ron ; bu t this neu- ron r e m a i n e d silent if the recept ive field center was t r aversed by a s t imulus wi th a con t inuous movement . The p h e n o m e n o n o f pa r t i cu l a r tec ta l cells r e spond ing well to j e r k y movemen t s and weak ly to s m o o t h mo-

t ion was also ob t a ined in frogs by Ingle (1977, per- sonal communica t ion ) .

References

Ewert, J.-P. : Verhaltensphysiologische Untersuchungen zum ,,stro- boskopischen Sehen" der Erdkr6te (Bufo bufo L.). Pfliiger~ Arch. 299, 158 166 (1968)

Ewert, J.-P. : The visual system of the toad: Behavioral and phys- iological studies on a pattern recognition system. In: The amphibian visual system. Fite, K.V. (ed.). New York, San Francisco, London: Academic Press 1976

Grfisser, O.-J., Finkelstein, D., Grtisser-Cornehls, U.: The effect of stimulus velocity in the response of movement sensitive neu- rons of the frog's retina. Pflfigers Arch. 300, 49-66 (1968)

Grfisser-Cornehls, U.: Response of movement-detecting neurons of the frog's retina to moving patterns under stroboscopic il- lumination. Pflfigers Arch. 303, 1-13 (1968)

Lettvin, J.Y., Maturana, H.R., McCulloch, W.S., Pitts, W.H.: What the frog's eye tells the frog's brain. Proc. Inst. Radio Engrs. N.Y. 47, 1940-1951 (1959)

Roth, G. : The role of stimulus movement patterns in the prey catching behavior of Hydromantes genei (Amphibia, Plethodon- tidae). J. comp. Physiol. 123, 261-264 (1978)