Neural computation of motion in the fly visual system: quadratic nonlinearity of responses induced by picrotoxin in the HS and CH cells

Abstract

1. A computational model accounting for motion detection in the fly was examined by comparing responses in motion-sensitive horizontal system (HS) and centrifugal horizontal (CH) cells in the fly's lobula plate with a computer simulation implemented on a motion detector of the correlation type, the Reichardt detector. First-order (linear) and second-order (quadratic nonlinear) Wiener kernels from intracellularly recorded responses to moving patterns were computed by cross correlating with the time-dependent position of the stimulus, and were used to characterize response to motion in those cells. 2. When the fly was stimulated with moving vertical stripes with a spatial wavelength of 5-40 degrees, the HS and CH cells showed basically a biphasic first-order kernel, having an initial depolarization that was followed by hyperpolarization. The linear model matched well with the actual response, with a mean square error of 27% at best, indicating that the linear component comprises a major part of responses in these cells. The second-order nonlinearity was insignificant. When stimulated at a spatial wavelength of 2.5 degrees, the first-order kernel showed a significant decrease in amplitude, and was initially hyperpolarized; the second-order kernel was, on the other hand, well defined, having two hyperpolarizing valleys on the diagonal with two off-diagonal peaks. 3. The blockage of inhibitory interactions in the visual system by application of 10-4 M picrotoxin, however, evoked a nonlinear response that could be decomposed into the sum of the first-order (linear) and second-order (quadratic nonlinear) terms with a mean square error of 30-50%. The first-order term, comprising 10-20% of the picrotoxin-evoked response, is characterized by a differentiating first-order kernel. It thus codes the velocity of motion. The second-order term, comprising 30-40% of the response, is defined by a second-order kernel with two depolarizing peaks on the diagonal and two off-diagonal hyperpolarizing valleys, suggesting that the nonlinear component represents the power of motion. 4. Responses in the Reichardt detector, consisting of two mirror-image subunits with spatiotemporal low-pass filters followed by a multiplication stage, were computer simulated and then analyzed by the Wiener kernel method. The simulated responses were linearly related to the pattern velocity (with a mean square error of 13% for the linear model) and matched well with the observed responses in the HS and CH cells. After the multiplication stage, the linear component comprised 15-25% and the quadratic nonlinear component comprised 60-70% of the simulated response, which was similar to the picrotoxin-induced response in the HS cells. The quadratic nonlinear components were balanced between the right and left sides, and could be eliminated completely by their contralateral counterpart via a subtraction process. On the other hand, the linear component on one side was the mirror image of that on the other side, as expected from the kernel configurations. 5. These results suggest that responses to motion in the HS and CH cells depend on the multiplication process in which both the velocity and power components of motion are computed, and that a putative subtraction process selectively eliminates the nonlinear components but amplifies the linear component. The nonlinear component is directionally insensitive because of its quadratic non-linearity. Therefore the subtraction process allows the subsequent cells integrating motion (such as the HS cells) to tune the direction of motion more sharply.