Texture-defined objects influence responses of blowfly motion-sensitive neurons under natural dynamical conditions

Abstract

The responses of visual interneurons of flies involved in the processing of motion information do not only depend on the velocity, but also on other stimulus parameters, such as the contrast and the spatial frequency content of the stimulus pattern. These dependencies have been known for long, but it is still an open question how they affect the neurons’ performance in extracting information about the structure of the environment under the specific dynamical conditions of natural flight. Free-flight of blowflies is characterized by sequences of phases of translational movements lasting for just 30–100 ms interspersed with even shorter and extremely rapid saccade-like rotational shifts in flight and gaze direction. Previous studies already analyzed how nearby objects, leading to relative motion on the retina with respect to a more distant background, influenced the response of a class of fly motion sensitive visual interneurons, the horizontal system (HS) cells. In the present study, we focused on objects that differed from their background by discontinuities either in their brightness contrast or in their spatial frequency content. We found strong object-induced effects on the membrane potential even during the short intersaccadic intervals, if the background contrast was small and the object contrast sufficiently high. The object evoked similar response increments provided that it contained higher spatial frequencies than the background, but not under reversed conditions. This asymmetry in the response behavior is partly a consequence of the depolarization level induced by the background. Thus, our results suggest that, under the specific dynamical conditions of natural flight, i.e., on a very short timescale, the responses of HS cells represent object information depending on the polarity of the difference between object and background contrast and spatial frequency content.

Motion as a source of environmental information: a fresh view on biological motion computation by insect brains

“…Here we want to take an alternative stance by proposing that these pattern-dependent modulations of the movement detector output do not reflect noise in the context of velocity coding. Rather, they can be interpreted as being relevant from a functional point of view, as they reflect potentially useful information about the environment and, thus, may be relevant for visually guided orientation behavior (Meyer et al, 2011 ; O’Carroll et al, 2011 ; Hennig and Egelhaaf, 2012 ; Schwegmann et al, 2014 ; Ullrich et al, 2014b ).…”

“…However, individual LWCs are far from being ideal for self-motion estimation as their receptive fields are spatially clearly restricted and show distinct spatial sensitivity peaks. Accordingly, they show pronounced response modulations even during constant-velocity motion resulting from textural features of the environment (Meyer et al, 2011 ; O’Carroll et al, 2011 ; Ullrich et al, 2014b ). In addition, the responses of LWCs provide information about the spatial layout of the environment—at least on a coarse spatial scale, but even on the short timescale of intersaccadic intervals: the intersaccadic response amplitudes evoked by ego-perspective movies were found to depend on the distance to the walls of the flight arena in which the corresponding behavioral experiments were performed or on objects that were inserted close to the flight trajectory (Boeddeker et al, 2005 ; Kern et al, 2005 ; Karmeier et al, 2006 ; Liang et al, 2008 , 2012 ; Hennig and Egelhaaf, 2012 ).…”

“…We can conclude from this experimental evidence that during translational self-motion as is characteristic of the intersaccadic flight phases of flies and bees that even motion sensitive cells with relatively large receptive fields provide spatial information about the environment. Although it is still not clear to what extent this information is exploited for behavioral control (see below), its potential functional significance is underlined by the fact that the object-induced responses observed during intersaccadic intervals are further increased relative to the background activity of the cell as a consequence of motion adaptation (Liang et al, 2008 , 2011 , 2012 ; Ullrich et al, 2014b ).…”