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First published online June 16, 2005
Journal of Experimental Biology 208, 2515-2532 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01640

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Habituated visual neurons in locusts remain sensitive to novel looming objects

John R. Gray

Department of Biology, University of Saskatchewan, Saskatoon, SK, Canada S7N 5E2

View larger version (27K): [in a new window]   Fig. 1. Experimental setup for presenting looming stimuli. (A) Left rear view of the experimental setup. The rear plate and left side panel of the base were removed from the figure to permit a clear view of the position of the locust in the setup. Computer-generated looming stimuli were projected onto a rear projection dome screen using a LCD projector. The locust was held in place on the inside of the dome with a rigid tether. A synchronization pulse from the stimulus was sent to the TTL input channel of the multichannel neurophysiological recording system. (B) Magnified view of area enclosed by the broken box in A showing the position of the multichannel probes below the tethered locust (see text for details of recording techniques). (C) Scaled images of the `locust' (top) and `bird' (bottom) looming stimuli. The `locust' was designed such that the two sets of wings rotated about the joint with the body in antiphase at 25 beats s-1, which emulated the flapping of real locust wings. The `bird' was designed with fixed wings to emulate a real bird during a gliding approach. For one sequence of approaches to each experimental animal the `bird' rotated ±45° about its longitudinal axis (arrows) at 1 roll s-1 to emulate internal object motion. (D) The angle of the experimental locust's field of view subtended by components of the looming stimuli identified in C. For both types of stimuli the object stopped 37 ms before collision. Lb, `locust' body: Lw, maximum width of `locust' wings; Bb, `bird' body; Bw, `bird' wing.

View larger version (16K): [in a new window]   Fig. 2. Identification of DCMD activity within the mesothoracic ganglion. (Ai) Multichannel silicon microprobes were inserted ventrally into the mesothoracic ganglion (outline shows scaled frontal view). Each of the probe's two tines contained two tetrode arrays (T1–T4). The arrangement of the recording sites was as follows: site 1–4 on T1, sites 5–8 on T2, sites 9–12 on T3, sites 13–16 on T4). Thus, sites 1–8 recorded activity from the left side of the ganglion and sites 9–16 recorded activity from the right side of the ganglion. (Aii) Recordings from a sample preparation showing waveforms overlaid in a 1.3 ms time window. The colours of the waveforms correspond to clusters identified in Aiii, which shows a plot of the peak of the waveforms of recording site 3 vs recording site 2 (see details in text for recording parameters). Well-defined clusters were easily identified in all preparations. (Aiv) 5 s time window showing the activity of the discriminated units during the presentation of a simulated looming bird. The blue and red units had the largest spike amplitudes and showed an increase in firing rate during an approach, characteristic of locust DCMDs. The arrow indicates time of collision. (B) Identification of the right and left DCMDs based on physiological responses to looming stimuli. The blue (right DCMD) and red (left DCMD, see Materials and methods for designation) rasters represent the spike times, during different approaches, of the units shown in A. In this example, each raster was time-aligned to the parameters of the approaching `bird', where 0=time of collision. The top two rasters show responses to a `bird' approaching from 0° azimuth (0°), which would be seen by both eyes. The middle rasters show responses to a `bird' approaching from +45° azimuth (+45°) and the bottom rasters show responses to a `bird' approaching from –45° azimuth (–45°). Because approaches from ±45° azimuth would occupy the field of view of the ipsilateral eye only, these criteria could be used to discriminate unambiguously right and left DCMD activity for all runs for each animal. Bb and Bw as in Fig. 1.

View larger version (32K): [in a new window]   Fig. 3. Quantitative measurements of DCMD firing parameters. This data shows one response of the right DCMD to a `bird' approaching from +45° azimuth. (Top) The raster plot shows the DCMD spike times. (Middle) A Gaussian smoothed (bin=50 ms) plot of the instantaneous firing rate (see text for details). (Bottom) The subtense angle of the `bird' body (Bb) and wing (Bw). From the rate histogram plots I measured the time and amplitude of peak firing (asterisk), the instantaneous spike rate 200 ms before collision (arrow), and the total number of spikes during each approach (see Materials and methods). For this example the DCMD produced 29 spikes and reached a peak firing rate of 165 spikes s-1 169 ms before collision. At this time the `bird wing' subtended approximately 25° of the right eye's field of view. The point at which the angle of the `bird' wing jumps by more than 3° is 125 ms before collision. Thus in this example the DCMD peak occurred 86 ms (or approximately 7 frames) before a proposed critical subtense angle jump of more than 3° (see Rind and Simmons, 1997).

View larger version (30K): [in a new window]   Fig. 4. Dishabituation of DCMD responses between presentations of approach sequences. (A) The number of DCMD spikes for each first approach according to the order of presentation of a sequence (i.e. the order of which the randomized sequences were actually presented, see Table 1). The number of spikes (mean ± S.D.) was lower for approaches of a `locust' than for a `bird'. A Kruskal–Wallis ANOVA on ranks showed that there were no significant differences in the number of spikes within an object type (i.e. `locust' or `bird'). In (B) the data were normalized to the first presentation of a particular object and trajectory. For example, the first approach for each sequence of a simulated locust approaching from 0° azimuth was normalized to the first time that approach was presented. If there were no confounding effects of incomplete dishabituation then the normalized values should not be different from 1. A Kruskal–Wallis ANOVA on ranks showed that there were no significant differences in the normalized number of spikes within an object type. These data show that the DCMDs were fully dishabituated prior to each presentation sequence. (See text for statistical parameters; bars with the same letters were not statistically different, N=11.)

View larger version (19K): [in a new window]   Fig. 5. DCMD responses to 30 consecutive approaches of a `locust' or `bird' at 34 s intervals. (A) Sample raster plots from one sequence of 30 approaches showing responses of the right DCMD to a `locust' (black) and a `bird' (red) approaching from +45° azimuth. (Bi) The peak spike rate, (Bii) the spike rate at t=–200 ms and (Biii) number of spikes decreased following the first approach of either a `locust' (black circles and line) or `bird' (red circles and line) and plateaued after 10 or 15 approaches. Data plotted (means ± S.D.) are from 9 animals. For clarity the S.D. is shown in only one direction. Mean values of each plot were well fit by a single exponential decay of the form y=y0+ae-bx. r2 values for each plot are indicated. Means were calculated from pooled right and left DCMDs (0° azimuth trajectories) and pooled ipsilateral DCMDs (±45° azimuth).

View larger version (19K): [in a new window]   Fig. 6. Assessment of whether DCMD habituation was the same for repeated presentations of a `locust' (black bars) and `bird' (open bars). The value of the 30th (habituated) approach was normalized to the first approach. Values are means ± S.D. A two-way ANOVA revealed that the object size or trajectory did not affect the peak spike rate. A `locust' approaching from 0° azimuth resulted in a greater decrease of the instantaneous spike rate 200 ms before collision than did a `bird' from the same trajectory or a `locust' approaching from ±45° azimuth (see text for statistical parameters; bars with the same letters were not statistically different, N=9). Comparisons were made within each graph.

View larger version (25K): [in a new window]   Fig. 7. DCMD responses to 17 consecutive approaches of a `locust' (black) or `bird' (red) at 4 s intervals. Approach 16 is the same object approaching along a different trajectory. (A) Sample raster plots of the right DCMD to 17 approaches of a `locust' and `bird' showing a stronger response to approach 16 (arrows). In this example approaches 1–15 and 17 are from 0° azimuth and approach 16 is from +45° azimuth. (Bi–iii) Data (N=11) were plotted as in Fig. 5 except that the curve was fit for approaches 1–15. For clarity the S.D. is shown in only one direction.

View larger version (45K): [in a new window]   Fig. 8. Habituated DCMDs (approach 15) were able to respond to objects approaching along a new trajectory (approach 16) with a significantly higher peak spike rate, spike rate 200 ms before collision and number of spikes. The new trajectory did not dishabituate the response to the original trajectory (approach 17). (See text for statistical parameters, significance assessed as in Fig. 6). `locust', black bars; `bird', open bars. Data are plotted as the mean ± S.D. (N=11).

View larger version (15K): [in a new window]   Fig. 9. DCMD responses to 17 consecutive approaches of a `locust' (black rasters) or `bird' (red rasters) at 4 s intervals. Approach 16 is a new object [`bird' following `locust' (red arrow) or `locust' following `bird' (black arrow)] approaching along the same trajectory. All data plotted as in Fig. 7. (A) The habituated right DCMD responded more strongly to a `bird' (red arrow) than to a `locust' (black arrow) approaching from +45° azimuth. (Bi) The peak spike rate, (Bii) the spike rate 200 ms before collision and (Biii) the number of spikes increased only when the DCMD was presented with a new larger object (note approach 16, N=11). For clarity the S.D. is shown in only one direction.

View larger version (29K): [in a new window]   Fig. 10. Habituated DCMDs respond to a new, larger object. Data plotted as in Fig. 8. Note that the open bar for approach 16 is not significantly different from the habituated condition. Significance assessed and indicated as in Fig. 8.

View larger version (16K): [in a new window]   Fig. 11. (A) Regardless of the approach interval, the mean time of peak DCMD firing occurred earlier after repeated approaches of a `locust' from ±45 azimuth and was relatively insensitive to repeated approaches of either object from 0° azimuth or a `bird' from ±45° azimuth (N=11). For trajectories and intervals in which the time of the peak was invariant, it occurred 28±27 ms(mean ± S.D.) before collision of a `locust' and 50±40 ms before collision of a `bird'. For clarity the S.D. is shown in only one direction. r2 values as in Fig. 5. (B) The S.D. of time of peak firing was not affected by repeated presentations at 34 s intervals of a `locust' approaching along either trajectory or a `bird' approaching from 0° azimuth (left) whereas the S.D. increased during repeated approaches of a `bird' from ±45° azimuth (r=0.429, P=0.019). (Right) For approaches at 4 s intervals the S.D. was not affected by repeated presentations of a `locust' or `bird' from 0° azimuth whereas it decreased upon repeated approaches of a `locust' (r=–0.698, P=0.004) or `bird' (r=–0.551, P=0.033) from ±45° azimuth. For approaches from ±45° (4 s intervals) the rate of decrease of the S.D. (b from the single exponential decay function) was greater during repeated approaches of a `locust (b=0.390) compared to a `bird' (b=0.200).

View larger version (30K): [in a new window]   Fig. 12. Internal object motion does not affect the initial response or habituation of DCMDs to repeated looming stimuli. (Ai) Sample raster plots of sequences of 15 approaches (4 s intervals) of a `bird' from 0° azimuth (top rasters) or of a `bird' from 0° azimuth with an additional roll component (bottom rasters). The subtense angle of the `bird' wing (Bw) and `bird' body (Bb) during an approach (Aii, top) are the same for both stimulus types. The roll angle about the `bird's longitudinal axis during an approach is shown in (Aii, bottom). Note that the spike trains for each approach number were similar for each type of stimulus and that spike trains did not phase-lock to the roll angle. (Bi) The peak spike rate, (Bii) the spike rate 200 ms before collision and (Biii) the number of spikes of the pooled right and left DCMDs during approaches 1 and 15 were compared between the different stimulus types. There were no significant differences (Kruskal–Wallis ANOVA on ranks; see text) in any of the measured parameters compared during approach 1 or during approach 15. Data plotted are the mean ± S.D. (N=11; significant differences as in Fig. 6).