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First published online October 10, 2003

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Neural images of pursuit targets in the photoreceptor arrays of male and female houseflies Musca domestica

Brian G. Burton^* and Simon B. Laughlin

Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK

View larger version (21K): [in a new window]   Fig. 1. Stimulus parameters. (A) Target parameters. As seen at the eye, a target is described by its angular width x and angular speed . For a target of given absolute width b, these parameters correspond to a particular distance s and flight speed u. (B) Lines of constant target flight speed u (solid) and distance s (broken), in the plane of target angular speed and angular width x. (C) Target contrast C falls with distance because more distant targets appear smaller and suffer more optical blur. The effect is greater in females than in males. (D) Stimulus parameters. The light stimuli delivered to male (solid line) and female (broken line) photoreceptors, simulating a 3° target moving at 100 deg. s-1. Owing to superior optics, the male stimulus has a higher contrast C and a shorter width c at half maximum amplitude.

View larger version (31K): [in a new window]   Fig. 2. Male and female pursuit responses. Traces show the mean response (N=25) of a male (blue) photoreceptor and a female (red) photoreceptor to a simulated moving target of specified angular width and angular speed. Vertical range is 24 mV. Traces are centred on the peak of the male response and the time axes are scaled by male response duration. The top left plot shows the responses of the same cells to conventional white-noise stimuli (contrast, 25%; cut-off frequency, 400 Hz), male response (blue) above, female response (red) below.

View larger version (20K): [in a new window]   Fig. 3. Target detection. Signal detection analysis of predicted target responses at small target widths (large distances) in 7 male and 7 female photoreceptors. The signal-to-noise ratio, d', measures mean response amplitude divided by photoreceptor noise S.D. after filtering responses to suppress noise. Values are means ± S.D. Also plotted is an error line that shows the value of d' (3.29) at which an ideal observer would incorrectly identify signal-present and signal-absent trials 5% of the time in an experiment in which half the trials do not contain a target and when the noise is Gaussian.

View larger version (35K): [in a new window]   Fig. 4. Effects of angular target speed on response amplitude and image blur. (A,B) Mean response amplitudes V of 7 male (A) and 7 female (B) photoreceptors to simulated target stimuli, plotted against angular target speed . The male response is larger than the female response and demonstrates an optimum angular speed that increases with target size. (C,D) Mean angular response width v of the same male (C) and female (D) photoreceptors to simulated target stimuli, plotted against angular target speed . At low speeds, response widths are less than the widths of the targets (indicated by dotted lines), especially in the male. At high speeds, response width increases with speed (motion blur).

View larger version (27K): [in a new window]   Fig. 5. Effects of absolute target speed on response amplitude and image blur. (A,B) Mean response amplitudes V of 7 male (A) and 7 female (B) photoreceptors to simulated target stimuli, plotted against absolute target speed u. The optimum male response occurs at speeds between 10 cm s-1 and 80 cm s-1, for targets at distances of up to 33 cm. (C,D) Mean spatial blur factor v/x of the same male (C) and female (D) photoreceptors to simulated target stimuli, plotted against absolute target speed u. The male achieves blur factors of less than 1 for slow moving targets at distances of <15 cm. Motion blur begins in both sexes when the target is travelling at approximately 50 cm s-1.

View larger version (25K): [in a new window]   Fig. 6. Effects of stimulus duration on response amplitude and image blur. (A,B) Mean contrast amplification V/C of 7 male (A) and 7 female (B) photoreceptors to simulated target stimuli plotted against stimulus duration c. Males preferentially amplify high contrast (near) stimuli. The amplification performed by the female photoreceptor is less powerful than that of the male photoreceptor and exhibits non-linear contrast gain at only the longest durations. Below 4 or 5 ms in both sexes, the response decreases as stimulus power declines. (C,D) Mean temporal blur factor v/c of the same male (C) and female (D) photoreceptors to simulated target stimuli, plotted against stimulus duration c. The male blur factor is always less than the female's for stimuli of comparable contrast, especially at high contrast. Motion blur occurs at stimulus durations below 10 ms.

View larger version (38K): [in a new window]   Fig. 7. Neural images of a moving target. (A-C) Contour plots of the angular distribution of relative intensity from a 3.44° target, seen at the eye (A) and after blurring by male (B) and female (C) optics. Contour lines are spaced at intervals of 0.1. The lines on far right indicate half-width. (D,E) Snapshots of the distribution of photoreceptor voltage responses to the same target moving at 180 deg. s-1 from left to right as reconstructed for male (D) and female (E) retinas. Crosses indicate the current position of the target. (F,G) Sampled retinal images of the moving target for male (F) and female (G) retinas. Colour patches represent the instantaneous voltage responses of individual photoreceptors separated at angles appropriate for males (1.6°) and females (2.5°).

View larger version (17K): [in a new window]   Fig. 8. White-noise analysis does not predict pursuit responses. (A-F) Responses (solid line) of a male photoreceptor to selected pursuit stimuli are compared with those predicted from first-order (dotted line) and second-order (broken line) kernels from white-noise analysis. The voltage scale for all plots is the same (scale bar in A). The kernel predictions often underestimate the true response and comparison of (E) and (F) suggests that stimulus duration, not just the final predicted potential, is responsible for these differences.