Visual Neuroscience (1990), 4, 579-584. Printed in the USA. Copyright © 1990 Cambridge University Press 0952-5238/90 $5.00 + .00 Shift of edge-taxis to scototaxis depends on mean luminance and is predicted by a matched filter theory on the responses of fly lamina LMC cells R. B. PINTER, 1 D. OSORIO, 2 AND M. V. SRINIVASAN 2 1 Department of Electrical Engineering, The University of Washington, Seattle, and 2 The Australian National University, Centre for Visual Sciences, Canberra (RECEIVED March 21, 1989; ACCEPTED March 14, 1990) Abstract The strength of the flanking inhibitory regions of the receptive fields of fly lamina cells (LMC) decreases as the mean luminance is lowered. Simultaneously, the biphasic temporal flash (impulse) response of the lamina cells becomes monophasic on lowering luminance. For a moving-edge stimulus at high mean luminance, this implies that the spatial integration by the lamina cell yields a temporal waveform which is congruent to the waveform of the temporal impulse response of the lamina cell. In other words, the temporal waveform generated by the moving edge is matched to the temporal waveform most preferred by the lamina cell. The edge is the stimulus causing the largest amplitude response at high (above 1 cd/m 2 ) levels of luminance. On lowering luminance, the now monophasic nature of the spatial and temporal impulse responses of the lamina gives a preference not for the edges but for the center of a uniform region. We describe this theory and its behavioral corroboration in walking flies (Lucilia cuprina). Keywords: Mean luminance, Fly lamina cells, Scototaxis, Flanking inhibitory regions, Lateral inhibition, Edge response, Edge taxis Introduction Lateral inhibition and excitatory center-surround receptive fields of visual neurones are well known, and corollary linear theories of physiological image processing have been extensively explored (Ratliff et al., 1969; Kelly, 1975). Among the many nonlinearities of visual systems, a well-behaved, smooth non- linearity in many visual cells is found by varying the mean lu- minance and presenting stimuli of given contrast at each given luminance. Both temporal response characteristics (impulse re- sponse and frequency responses; insect photoreceptors, Pinter, 1972; fly lamina LMC cells, Laughlin et al., 1987; Laughlin & Osorio, 1989, and this study, Fig. 1) and spatial response char- acteristics (insect medulla neurone HI, Srinivasan & Dvorak, 1980; insect lamina LMC cells, Dubs, 1982) vary with change of mean luminance such that a sharpening, or increase of band- width of the temporal and spatial response characteristics, oc- curs for increased mean luminance. These features are parallel with those found psychophysically (DeLange, 1958, temporally; Patel, 1966 and Kelly, 1975, spatially) and may imply a mech- anism to employ the greater information capacity in the larger number of available photons at higher mean luminance (Srini- vasan et al., 1982; Pinter, 1984, 1985). However, in fly lamina Reprint requests to: R. B. Pinter, Department of Electrical Engineer- ing, University of Washington FT-10, Seattle, WA 98195, USA. LMC cells we find there may be a more specific function for these spatio-temporal changes on raising of mean luminance: shift of LMC cell response preference away from the center of a uniform bright or dark region (or "blob") to preference for moving edges. This change in visual interneuron properties is a possible explanation of the flies' behavioral preference for edges at high luminance. Since the lamina is the most peripheral integrative neuropil, it is certainly possible that in more central neuropil parallel changes occur on change of mean luminance, for which there is already some clear evidence (Srinivasan & Dvorak, 1980). Thus, we do not suggest that only the lamina cells determine the walking behavior and preference for edges. Rather, the LMC luminance-dependent change of function cor- roborates the behavior and suggests a model for the luminance- dependent functions of more central cells. We have noticed that there is a similarity in the changes of the spatial receptive field and the temporal impulse (short flash) response of fly lamina LMC cells on change of mean luminance such that at high luminances the spatial receptive field possesses lateral surrounds antagonistic or inhibitory to the central re- sponse, and the temporal impulse response is biphasic. This matches the spatial and temporal responses to a moving edge which is thus regarded as the optimal stimulus of a light adapted LMC. On lowering the mean luminance, the biphasic nature of both spatial and temporal response characteristics disappears, and the match between the spatial and the temporal character- 579