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'

Abstract

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* greater than Rt*), thus displaying 'head preference'. If the contrast-direction is reversed (w/b), the stripe's trailing edge is preferred (Rl* less than 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 degrees X 30 degrees 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 in tectal neurons and to stimulus area evaluation and (in combination with R4 output) sensitivity for moving background structures in pretectal neurons.(ABSTRACT TRUNCATED AT 400 WORDS)