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First published online March 17, 2006
Journal of Experimental Biology 209, 1251-1260 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02127

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Representation of behaviourally relevant information by blowfly motion-sensitive visual interneurons requires precise compensatory head movements

R. Kern^1,*, J. H. van Hateren² and M. Egelhaaf¹

¹ Department of Neurobiology, Faculty for Biology, Bielefeld University, Bielefeld 33501, Germany
² Department of Neurobiophysics, University of Groningen, Groningen 9747 AG, The Netherlands

View larger version (45K): [in a new window]   Fig. 1. (A) Time course of head (blue) and body (red) yaw angle exemplifying the saccadic flight style of blowflies. Positive slopes denote leftward turns, i.e. turns leading to optic flow into the preferred direction of the right horizontal system equatorial neuron (HSE). The free-flight data were recorded in an arena with dimensions of about 40x40x40 cm3, with images of herbage covering the walls. Arrows are pointing towards instances where slow, intersaccadic angular head movements were against (left arrow) or with (right arrow) the direction of previous saccadic turns. (Inset) Sections of yaw traces, vertically enlarged (scale bar, 20°). (B,C) Average membrane potential of an HSE-cell in the right brain hemisphere in response to the optic flow corresponding to (B) head or (C) body movements, the yaw component of which is shown in A (N=9 responses each). Broken lines denote resting potential; responses are shifted backwards in time to account for response latencies and low-pass filtered with a Gaussian, standard deviation of 3 ms. Upward and downward deflections of the yaw angle in A correspond to optic flow in the preferred and null direction of the analysed neurons, respectively.

View larger version (26K): [in a new window]   Fig. 2. Average coherence (± s.e.m.) of sideward angular velocity (solid line) and yaw velocity (broken line) with the subtracted responses of right and left horizontal system equatorial neuron (HSE) (N=4), intersaccadic parts of stimulus and response only. Responses to optic flow based on head orientation (A) or body yaw (B). Sideward is perpendicular to the head's plane of symmetry. Behavioural data used for reconstruction of visual stimuli are based on two flights originating from different flies.

View larger version (41K): [in a new window]   Fig. 3. (A) Yaw velocity of head (blue), body (red) and headified (yaw-tuned) body (green). This flight segment corresponds to the segment for which yaw angles are shown enlarged in Fig. 1A inset. (B) Same as A, vertically zoomed. Yaw velocities in A and B were obtained from the differential rotation matrix of the body or head (van Hateren and Schilstra, 1999) and were low-pass filtered with a Gaussian (standard deviation 3 ms) to reduce measurement noise. (C) Average response of an horizontal system south neuron (HSS) cell to optic flow corresponding to yaw velocities shown in A. Broken line at 0 mV corresponds to the resting potential; responses are shifted backwards by 22.5 ms to account for response latencies and low-pass filtered with a Gaussian, standard deviation 3 ms.

View larger version (28K): [in a new window]   Fig. 4. (A) Probability density function at the intersaccadic intervals of head yaw (blue), body yaw (red) and tuned body yaw (green) velocity. (B–D) Power spectra of sideward (solid) and yaw (broken) angular velocity for body yaw velocity (B), head yaw velocity (C) and tuned body yaw velocity (D); power spectral densities were calculated for the intersaccadic intervals using an algorithm by (Scargle, 1989; see also Kern et al., 2005b). Sideward is perpendicular to the head's plane of symmetry. Since the optic flow resulting from translational movements depends on the distance to environmental objects, sideward velocities of the fly were converted to angular velocities by multiplying by the nearness (equal to the inverse of the distance) (Koenderink, 1986) averaged over the trajectories and over the receptive fields of the neuron (average nearness: 7.14 m–1, corresponding to a typical distance to the arena wall of 0.14 m). Data based on two flights originating from different flies. Note that the y-axis in B is scaled differently from those in C and D.

View larger version (22K): [in a new window]   Fig. 5. Algorithm to obtain a headified body orientation from the measured body yaw. See the text for an explanation.

View larger version (33K): [in a new window]   Fig. 6. Coherence of sideward angular velocity (solid line) and yaw velocity (broken line) with the subtracted responses of right and left horizontal system equatorial neuron (HSE) (A–C), horizontal system south neuron (HSS) (D–F) and dorsal centrifugal horizontal neuron (DCH) cell (G–I), intersaccadic parts of stimulus and response only. Responses to optic flow based on head (A,D,G), body (B,E,H) or yaw tuned body (C,F,I) movements. Single cell results, based on 3–8 stimulus repetitions of two different flights. Sideward is perpendicular to the head's plane of symmetry.

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