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Effects of stretch receptor ablation on the optomotor control of lift in the hawkmoth Manduca sexta

Mark A. Frye

University of Washington, Department of Zoology, Box 351800, Seattle, WA 98195-1800, USA

View larger version (32K): [in a new window]   Fig. 1. The arena for tethered flight. The moth was tethered behind a translucent screen subtending 180° at the eye. A pattern of horizontal stripes was projected onto the screen and moved vertically by a computer-controlled servomotor (not shown). A laser system (inset) tracked up–down displacement of the tether and was calibrated to net vertical force (lift); an LED/photodetector pair tracked fore–aft displacement and was calibrated to horizontal force (thrust). A laser beam focused into a two-dimensional ‘sheet’ of light was cast across the abdomen onto an optoelectronic sensor to track angular deflections of the abdomen. A CCD camera was oriented orthogonal to the longitudinal axis of the moth and recorded wing motion at 500 frames s–1.

View larger version (31K): [in a new window]   Fig. 2. Surgical ablation of the metathoracic wing hinge stretch receptor (SR). The stretch receptor sensory terminals are embedded within the subalar membrane between the metathoracic epimeron and subalar sclerite. The stretch receptor axon initially passes through a nerve composed of only its axon. A tiny incision was made in the soft cuticle (represented by the box) just dorsal to the axillary cord, and the stretch receptor was ablated by cutting its peripheral nerve. Nerve IIINb1 contains the axons from a hair plate on the scutum, a chordotonal organ and the stretch receptor.

View larger version (20K): [in a new window]   Fig. 3. Lift evoked by the hawkmoth in response to large-field image motion. Lift is defined as net vertical force; zero lift corresponds to mean body weight. The image was oscillated up and down in steps of constant velocity (C). Resultant lift responses, averaged across animals, are plotted for intact moths (A) (N=9) and for moths with stretch receptors (SRs) ablated (B) (N=10). Thick lines plot mean force, and thin lines plot ± S.D.

View larger version (13K): [in a new window]   Fig. 4. For one test velocity (400° s–1), responses to a sham ablation were tested. Lift modulation corresponds to the amount of lift evoked in response to a step in image speed (see Materials and methods). The surgical sham had no effect on mean lift modulation, while stretch receptor ablation reduced lift modulation to approximately 30 % of the intact response (Student’s t-test, *P<0.05, N=9 intact, N=10 ablated and N=5 sham). Values are means ± S.D.

View larger version (18K): [in a new window]   Fig. 5. Lift in response to large-field image motion for test sequences of varying velocity (indicated numerically in each plot). Mean lift is plotted for the adaptation cycle preceding the test sequence. Image position is illustrated schematically at the bottom of the figure as a time reference. Data for intact moths are plotted in blue (N=9) and for stretch-receptor-ablated moths in red (N=10).

View larger version (15K): [in a new window]   Fig. 6. Mean lift modulation versus angular velocity (image speed). Data from intact moths are plotted in blue (N=9) and from stretch-receptor-ablated moths in red (N=9). Values are means ± S.D.

View larger version (14K): [in a new window]   Fig. 7. Abdominal deflections in response to large-field image motion. Averaged responses are plotted for intact (blue, N=3) and stretch-receptor-ablated moths (red, N=3).

View larger version (32K): [in a new window]   Fig. 8. Extracellular recordings of dorsolongitudinal (red) and dorsoventral (blue) muscle activity during tethered flight after a surgical sham (A) and after bilateral stretch receptor ablation (B). Stretch receptor (SR) ablation did not significantly influence the frequency of phase of activation in these muscles (see Results).

View larger version (38K): [in a new window]   Fig. 9. Wingtip projection during upward and downward image motion at 160° s–1. The two-dimensional projection of the wingpath is plotted for a single individual before (blue) and after (red) stretch receptor ablation and for downward (top row) and upward (middle row) image motion. The average wingpath evoked by upward image motion is shown in the bottom diagram (N=3). The data were digitized from video images recorded at 500 frames s–1.