Influence of environmental information in natural scenes and the effects of motion adaptation on a fly motion-sensitive neuron during simulated flight

Abstract

Gaining information about the spatial layout of natural scenes is a challenging task that flies need to solve, especially when moving at high velocities. A group of motion sensitive cells in the lobula plate of flies is supposed to represent information about self-motion as well as the environment. Relevant environmental features might be the nearness of structures, influencing retinal velocity during translational self-motion, and the brightness contrast. We recorded the responses of the H1 cell, an individually identifiable lobula plate tangential cell, during stimulation with image sequences, simulating translational motion through natural sceneries with a variety of differing depth structures. A correlation was found between the average nearness of environmental structures within large parts of the cell's receptive field and its response across a variety of scenes, but no correlation was found between the brightness contrast of the stimuli and the cell response. As a consequence of motion adaptation resulting from repeated translation through the environment, the time-dependent response modulations induced by the spatial structure of the environment were increased relatively to the background activity of the cell. These results support the hypothesis that some lobula plate tangential cells do not only serve as sensors of self-motion, but also as a part of a neural system that processes information about the spatial layout of natural scenes.

Keywords: Adaptation; Contrast; Fly; Natural images; Nearness; Neural activity; Spatial vision.

Fig. 1.. Examples of the natural images recorded in different natural environments and corresponding nearness maps.

(A–D) Grayscale panoramic images of the natural scenes. Clearing in the forest with near trunks (A), near branches (B) and distant trees (C), open field (D). (E–H) Color-coded nearness maps of the same scenes.

Fig. 2.. Outline of the two types of stimulus sequences employed in the analysis.

(A) Environment information stimuli; (B) adaptation stimuli. The different sections of the stimuli are marked as colored blocks (periods of translational motion: red, accelerating/decelerating rotational motion: black, constant rotational motion: blue, no-motion: white).

Fig. 3.. Time course of the nearness and comparison to the cell response during the translation sequence of an example natural scene (see also Fig. 1B).

(A) Color-coded panoramic nearness map showing local nearness values. Analysis window depicted as a grey square. (B) Sections of the nearness map showing the changing local nearness values within the analysis window during the translation sequence. (C) Time course of the ‘time-dependent nearness’ averaged across the analysis window (black solid line) and time-averaged nearness (grey dashed line). (D) Time course of the cell response of a single cell (black solid line), normalized to the response to the characterizing stimulus, averaged across repetitions of the translation sequence and average cell response during translation sequence (grey dashed line). Cell response sampled at 200 Hz.

Fig. 4.. Dependence of the average cell response on the time-averaged nearness for the different natural sceneries.

Data obtained in different environments are indicated by different colors. Horizontal bars: standard deviation of the ‘time-dependent nearness’ during the translation sequence within a given scenery. Vertical bars: standard deviation of response modulations obtained during the translation sequence in a given scenery. Corresponding mean values are given by the crossing of the horizontal and vertical bars. Regression line (red dashed line) illustrating the relation between nearness values and cell responses.

Fig. 5.. Dependence of the average cell response on the time-averaged RMS contrast of different natural scenes.

Data obtained in different environments are indicated by different colors; scenes are specified by the same colors as in Fig. 4. Horizontal bars: standard deviation of the ‘time-dependent RMScontrast’ across the translation sequence in a given scenery. Vertical bars: standard deviation across time of response modulations obtained during the translation sequence in a given scenery. Corresponding mean values are given by the crossing of the horizontal and vertical bars. Regression line (red dashed line) illustrating the relation between contrast values and cell responses.

Fig. 6.. Motion adaptation reduces the average cell response to the translation sequence over time.

Data obtained for the different natural scenes are indicated by different colors; colors specify different scenes compared to previous figures. The cell response is time-averaged across single translation sequences and normalized by the value obtained for the first translation sequence (values of the first translation sequence specified in the figure inset, error bars: standard error of the mean across cells). Time is indicated as the number of the translation sequence and the markers of single scenes are slightly shifted along the x-axis to enhance visibility.

Fig. 7.. Motion adaptation increases time-dependent response modulations (TDRM) relatively to the average cell response.

TDRM normalized to the value obtained for the first translation sequence of two selected scenes (see Materials and Methods), the scenes are plotted in the same color as in Fig. 6. Error bars: standard error of the mean across different cells. Time is indicated as the number of the translation sequence and the markers of single scenes are slightly shifted along the x-axis to enhance visibility.