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Recurrent Inversion of Visual Orientation in the Walking Fly, Drosophila melanogaster


Bülthoff,  HH
Department Human Perception, Cognition and Action, Max Planck Institute for Biological Cybernetics, Max Planck Society;

Götz,  KG
Neurophysiologie des Insektenverhaltens, Max Planck Institute for Biological Cybernetics, Max Planck Society;

Herre,  M
Max Planck Institute for Biological Cybernetics, Max Planck Society;

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Bülthoff, H., Götz, K., & Herre, M. (1982). Recurrent Inversion of Visual Orientation in the Walking Fly, Drosophila melanogaster. Journal of Comparative Physiology, 148(4), 471-481. doi:10.1007/BF00619785.

Movement-induced visual orientation in flies depends largely upon predictable responses which establish simple ldquooptomotor balancerdquo or complex ldquopseudo searchrdquo in the appropriate visual environment. Less conspicuous course diverting spontaneous actions of the flies become important in pattern-induced visual orientation. The apparently stochastic spontaneous actions of the houseflyMusca domestica still allow powerful probabilistic predictions of orientation during stationary flight (Reichardt and Poggio 1981). The predominance of non-stochastic spontaneous actions such as ldquobody saccadesrdquo, focussing and shift of ldquovisual attentionrdquo, plasticity of response components etc. in the fruitflyDrosophila melanogaster (Heisenberg and Wolf 1979–1980) accounts for complementary behavioural options which reduce the relevance of probabilistic predictions of orientation in this fly. The conjecture of ldquocomplementary optionsrdquo is based on a striking antagonism between orientation towards a visual object (fixation), and orientation in the opposite direction (anti-fixation), in the walking fly. Forced choice in a multiple-Y-maze quite definitely elicits fixation in the wild type, and antifixation in the ldquooptomotor blindrdquo mutantomb H31 (Fig. 3). However, these effects cannot be attributed to a continuous predominance of attraction in the wild type and repellence in the mutant. This is shown under comparable conditions of free choice in an arena: The flies of either strain alternate between fixation and anti-fixation of an inaccessible visual object (Fig. 4a), and keep running to and fro between two of these objects in ldquoBuridan's paradigmrdquo (Fig. 4b, c), even if the objects are not alike (Fig. 4d). The sequence of approach, retreat and transition may be repeated a few thousand times to the point of exhaustion (Fig. 5). The process resembles the recurrent alternation of ambiguous figures such as the Necker cube in human perception. The recurrent transition between competitive objects counteracts the accumulation of spontaneous preferences, and is likely to explain the apparent lack of pattern-discrimination under operant and non-operant conditions of continued free choice inDrosophila. The conspicuous dichotomy of fixation and anti-fixation in the same environment is, as yet, incompatible with the phenomenological theory of visually controlled orientation in larger flies.