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First published online November 1, 2006
Journal of Experimental Biology 209, 4464-4474 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02560

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A motion-sensitive neurone responds to signals from the two visual systems of the blowfly, the compound eyes and ocelli

Matthew M. Parsons^1,*, Holger G. Krapp² and Simon B. Laughlin¹

¹ Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK
² Department of Bioengineering, Imperial College London, South Kensington Campus, London, SW7 2AZ, UK

View larger version (51K): [in a new window]   Fig. 1. Photograph (A) and line drawing (B) of the rear aspect of the head capsule of Calliphora vicina. Because the ends of the two optical fibres almost touch the lateral ocelli, their light outputs (blue circles in A) do not overlap. The cuticle of the posterior face of the head capsule is cut away to expose the right-hand lobula plate, and the midbrain cavity, in which the ocellar nerve connects the ocellar neuropil with the brain. Scale bar, 500 µm. CEye, compound eye; LLOc, left lateral ocellus; RLOc, right lateral ocellus; OcN, ocellar nerve; LP, lobula plate.

View larger version (15K): [in a new window]   Fig. 2. The receptive field organisation and morphology of the V1 neurone [receptive field modified from Krapp et al. (Krapp et al., 2001)]. The orientation and length of each arrow in the vector map indicates the local directional motion preference and sensitivity, respectively. The map resembles the optic flow pattern generated by a rotation of the head about an axis approximately midway between pitch and roll (nodes at 45° and -135° azimuth). The grey box shows the approximate area and position of the display monitor we used for stimulating the compound eye. Inset: A schematic drawing of the fly brain, with a camera lucida drawing of a stained V1 neurone on the right-hand side (courtesy of Klaus Hausen). The approximate electrode position is indicated by the open arrowhead. Scale bar, 200 µm.

View larger version (50K): [in a new window]   Fig. 3. The response of V1 neurone to stimulation of the ocelli (A-C) and compound eyes (D-F) before (blue curves) and after (red curves) cauterisation of the ocellar nerve. The coloured curves show instantaneous spike rates (ISRs) averaged over 563 trials, and overlay extracellular recordings of V1's spike activity during a single trial. (A) ISR and representative recording before cauterising the ocellar nerve (scale bar, 15 µV). The grey shading indicates variability of ISR, ±1 s.e.m. The baseline of the extracellular recording indicates the mean spontaneous spike rate. (B) Stimulus presented to the right and left lateral ocelli. LED intensity difference=(left LED output-right LED output); Imax, max LED output. The dots show illumination switching between left and right ocelli as the LED intensity difference switches from Imax to -Imax. (C) Greatly reduced activity in V1 after cauterising the ocellar nerve, traces as in A. (D) ISR recorded in response to compound eye stimulation before cauterisation of the ocellar nerve. Traces as in A and C, but variability (±1 s.e.m.) is shown as a white band against the background of recorded spikes. (E) Compound eye stimulus: a horizontal sinusoidal grating (spatial frequency=0.63 cycles deg.-1) moving in V1's preferred direction, vertically downwards at 40 deg. s-1. Grating contrast was progressively increased over each trial to drive V1 over its full range of spike rate. (F) Response to compound eye stimulus after cauterisation of the ocellar nerve. The complete set of experiments was performed with five animals, giving a total of 563 trials for each stimulus protocol.

View larger version (11K): [in a new window]   Fig. 4. Response of V1 neurone to repetitive stimulation of the lateral ocelli, showing that a switch in illumination from right to left ocellus generates a phase locked spike in V1, whose jitter increases over successive repetitions. (A) Responses averaged over 29 stimulus trials in a single animal; black line, peristimulus spike time histogram (10 ms bins); grey trace, instantaneous firing rate, as described in Materials and methods. (B) Raster plot of spikes recorded in 20 of the trials. (C) Time course of ocellar stimulation; LED intensity difference=(left LED output-right LED output); Imax, max LED output.

View larger version (13K): [in a new window]   Fig. 5. The time course of the response of V1 neurone to a step change in ocellar light intensity (A,B), and a sinusoidal change (C,D). (A,C) Solid black lines: instantaneous firing rates averaged over 520 stimulus cycles; horizontal red lines: corresponding post-stimulus spike time histogram (5 ms bins); broken blue line: instantaneous firing rate of spontaneous activity, obtained during periods of zero stimulation between trials. (B,C) Time course of stimuli: LED intensity difference = (left LED output-right LED output); Imax, max LED output. Stimuli were applied in 40 blocks of 15 consecutive cycles. The blocks were separated by 2.5 s. The first and last cycle of each block was discarded to give 520 cycles.

View larger version (18K): [in a new window]   Fig. 6. The time course and latencies of the responses of 10 V1 neurones to step ocellar stimuli. (A) Instantaneous firing rates from 10 neurones arranged according to the latency of peak activity, tpeak. Data were averaged over more than 100 trials for each animal, the scale bar shows 100 spikes s-1. Blue broken lines indicate the spontaneous firing rate. (B) Stimulus sequence presented in each trial; LED intensity difference=(left LED output-right LED output); Imax, max LED output. (C) The latency of peak activity plotted against spontaneous firing rate. Red dots: latency versus spontaneous rate for the 10 neurones shown in A; blue crosses: the reduced peak latencies recorded when five of these cells were driven at >250 spikes s-1 by stimulating the compound eye. The vertical bars indicate a significant reduction of latency in each cell.

View larger version (21K): [in a new window]   Fig. 7. The response of V1 neurone to ocellar stimuli that changed intensity at different rates. (A) V1 responses at six rates of change; black lines: instantaneous firing rates (see Materials and methods), scale bar, 50 spikes s-1; red lines: peristimulus spike histograms (5 ms bins); grey lines; time courses of the intensity changes, plotted as LED intensity difference=(left LED output-right LED output), scale bar, 2Imax. Stimuli ramped from -Imax to Imax and then back to -Imax, where Imax=max LED output. (B) The relative modulation, Rmod of V1 (see main text) plotted against the rate of change of ocellar intensity, expressed as Imax s-1. The data have been normalised to the range of responses between that elicited by a step stimulus (maximum Rmod) and by zero stimulus (minimum, but non-zero Rmod).

View larger version (69K): [in a new window]   Fig. 8. The response of V1 neurone to combined stimulation of the ocelli and compound eye. (A) The instantaneous firing rate of V1 during stimulation of both the ocelli and compound eye (solid black line) and stimulation of the compound eye only (broken blue line). Data were averaged over 155 repetitions of the stimulus from a single animal. (B) Time course of ocellar stimulation. (C) Time course of the contrast of the compound eye stimulation. The data in A were obtained using a contrast increase of 0% to 20%. (D) The full set of 155 spike train rasters obtained during combined stimulation. (E) The peak ocellar-mediated change in V1 spike rate, R, plotted against the corresponding compound eye-only mediated value, at the time of each peak. Positive y-axis values therefore indicate ocellar-mediated excitation, whereas negative values indicate ocellar-mediated inhibition. To obtain enough data points, both the curves shown in C (0-10% and 0-20%) were used to stimulate the compound eyes. (F) Data from another animal (188 stimulus repetitions), presented in the same way as in E. Black lines in E and F are interpolant smoothing splines, each obtained using the same smoothing parameter (see Materials and methods).