Robust coding of ego-motion in descending neurons of the fly

Abstract

In many species, motion-sensitive neurons responding to optic flow at higher processing stages are well characterized; however, less is known how this representation of ego-motion is further transformed into an appropriate motor response. Here, we analyzed in the blowfly Calliphora vicina the visuomotor transformation from motion-sensitive neurons in the lobula plate [V2 and vertical system (VS) cells] onto premotor descending neurons [descending neurons of the ocellar and vertical system (DNOVS) cells] feeding into the motor circuit of the fly thoracic ganglion. We found that each of these cells is tuned to rotation of the fly around a particular body axis. Comparing the responses of presynaptic and postsynaptic cells revealed that DNOVS cells have approximately the same tuning widths as V2 and VS cells. However, DNOVS signals cells are less corrupted by fluctuations arising from the spatial structure of the visual input than their presynaptic elements. This leads to a more robust representation of ego-motion at the level of descending neurons. Thus, when moving from lobula plate cells to descending neurons, the selectivity for a particular optic flow remains unaltered, but the robustness of the representation increases.

Figure 1.

Ego-motion tuning of DNOVS cells. A, Schematic drawing of the investigated neural network. DNOVS cells receive motion information from lobula plate tangential cells (VS and V2) in the fly brain and convey the information among others onto neck motor neurons in the thoracic ganglion. B, Stimulus movies were generated by moving a virtual fly along or around the X-, Y-, or Z-axes in a virtual room. The virtual room was wallpapered with equally distributed squares. C, Movies were presented on the LED arena to a real fly while cells were recorded. D, DNOVS1 example responses to the three translations (lift, sideslip, and thrust) and to the three rotations (yaw, pitch, and roll). The movies were shown forward and backward corresponding to opposite movement directions of the fly, indicated by the black and red color. E, Mean responses ± SEM of DNOVS1 from n = 6 flies. F, Average peristimulus time histogram of the firing frequency of a DNOVS2 cell to the different movements (10 trials, bin size: 100 ms). G, Mean response ± SEM of DNOVS2 from n = 5 flies.

Figure 2.

Preferred axis of rotation of DNOVS1 and DNOVS2. A, Example responses of DNOVS1 to 12 different axes of rotation. B, Mean responses to 36 axes of rotation of DNOVS1 (n = 4 flies) and DNOVS2 (n = 3 flies), shown in color code. Red represents a depolarization of DNOVS1 or an increase of the firing rate of DNOVS2, blue a hyperpolarization. Black bar indicates the preferred axis of rotation.

Figure 3.

Preferred axis of rotation and tuning width of lobula plate tangential cells and DNOVS cells. A, Mean responses to 36 axes of rotation for 10 VS cells are shown color coded with red representing a depolarization and blue a hyperpolarization. The preferred axis of rotation (black ticks) shifts along the azimuth with increasing VS cell number. Data represents the mean of n number of flies for VS1 (n = 5), VS2 (n = 3), VS3 (n = 4), VS4 (n = 6), VS5 (n = 3), VS6 (n = 5), VS7 (n = 5), VS8 (n = 4), VS9 (n = 2), and VS10 (n = 1). B, Mean responses to 36 axes of rotation of n = 3 V2 cells. C, Tuning curve measured in a DNOVS1 and a VS7 neuron. The line drawn through the measured data of DNOVS1 indicates the fitted sinusoidal function. w indicates the tuning width defined as the part of the response tuning curve eliciting >50% of the maximum response. D, Tuning widths of DNOVS, VS, and V2.

Figure 4.

Robust coding of the axis of rotation in DNOVS1. A, Schematic drawing of the intracellular recording sites. VS6 and VS7 were recorded in the dendrite as well as in the axon, DNOVS1 in the dendrite. B, Picture of the stimulus movie called “artificial room” (movie can be seen in the supplemental material, available at www.jneurosci.org) representing a rotation around an axis at 30° azimuth. C–E, Average responses and membrane potential distributions of a VS6 dendrite, a VS6 axon, and a DNOVS1 cell to clockwise (blue) and counterclockwise rotation (red). Black distributions represent the variation of the resting membrane potential. F, G, Example membrane potential distributions of a VS7 dendrite and a VS7 axon. H, Mean Fano factors of DNOVS1, VS axon, and VS dendrite (pooled data from VS6 and VS7) for clockwise (blue) and counterclockwise (red) rotation. The mean values for DNOVS1 and VS axon/VS dendrite differed significantly. Data are from n = 7 DNOVS1, n = 7 VS axon (4 VS6, 3 VS7), and n = 12 VS dendrite (8 VS6, 4 VS7). I, Picture of the stimulus movie “natural room.” The Fano factors of DNOVS1 and VS axon/dendrite to rotations of the natural room differed significantly. Data are from n = 8 DNOVS1, n = 5 VS axon (2 VS6, 3 VS7), and n = 9 VS dendrite (5 VS6, 4 VS7). J, Stimulation with the “checkerboard room” elicited no observable difference in the responses of DNOVS1 and VS axon/dendrite. Data are from n = 5 DNOVS1, n = 3 VS axon (2 VS6, 1 VS7), and n = 8 VS dendrite (5 VS6, 3 VS7). Statistical tests were done between DNOVS1, VS axon, and VS dendrite (*p < 0.05, Wilcoxon rank sum test).