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Encoding properties of the wing hinge stretch receptor in the hawkmoth Manduca sexta

Mark A. Frye

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

View larger version (29K): [in a new window]   Fig. 1. Apparatus for recording extracellular stretch receptor activity during flight. Tethered moths were placed within a closed-circuit open-throat wind tunnel 11 cm in diameter. Windspeed was set at 1.5 m s–1. A laser focused into a two-dimensional ‘sheet’ of light projected across the right wing, casting a shadow onto an optoelectronic sensor. The sensor circuit produced a voltage linearly proportional to the elevation of the wing. During flight, in vivo deformation of the subalar sclerite (with reference to the immobile epimeron) was tracked with a high-speed CCD camera fitted with a macro lens. The hindwing stretch receptor (SR, inset) sensory dendrites ramify within the soft membrane spanning the cuticle of the subalar sclerite and epimeron. A small incision (box) in the soft cuticle was made between the metathoracic scutum and hindwing axillary cord. The peripheral stretch receptor nerve was fixed in a hook electrode. The electrode and ground reference wires were glued to the scutum with a droplet of beeswax/rosin mixture.

View larger version (29K): [in a new window]   Fig. 2. Apparatus used to deliver controlled deformation to the stretch receptor (SR) and record subsequent extracellular activity. A chart recorder pen-motor was used as a stretch actuator and force transducer (see Materials and methods). An armature linked to the motor was glued to the subalar sclerite with cyanoacrylate adhesive. The stretch delivered to the tissue was tracked with an LED/photodetector pair, which produced a voltage linearly proportional to the position of the armature. Activity of the stretch receptor was recorded with a stainless-steel hook electrode.

View larger version (13K): [in a new window]   Fig. 3. In vivo deformation of stretch receptor tissue (subalar membrane). The locations of markers placed on the moving subalar sclerite and the immobile epimeron were recorded and digitized at 500 frames s–1 during tethered flight. Filled symbols indicate the linear distance between the markers in successive video frames. A sine wave (solid line) was fitted to the data using a Simplex minimization routine written in Matlab (see Materials and methods). Note that there are periodic ‘gaps’ in the data series that correspond to times during which the downstroke of the wing occluded the view of the camera.

View larger version (11K): [in a new window]   Fig. 4. Stretch receptor (SR) activity in tethered moths. At rest, the stretch receptor discharges tonically (A), and during flight it fires a phasic burst of spikes near the dorsal stroke reversal (B). The small unit active between stretch receptor bursts is cross-talk from a hindwing depressor muscle.

View larger version (13K): [in a new window]   Fig. 5. During tethered flight, the number of spikes per stretch receptor burst increases with total wing elevation. Individual wingstrokes were segregated according to the number of stretch receptor spikes they evoked. Non-sequential histograms of relative wing elevation (see Materials and methods for definition) are plotted for bursts containing one, two, three or four spikes. While the distributions appear ‘noisy’, mean wing elevation increases significantly from 71 to 79 % of maximal wing elevation (ANOVA, F=85.7, P<0.001). This data set comprises 1507 wing strokes from a single flight bout.

View larger version (14K): [in a new window]   Fig. 6. The first stretch receptor (SR) spike is tightly tuned to the relative degree of wing elevation. Non-sequential histograms of wing position (see Materials and methods for definition) at the first stretch receptor spike are plotted for two moths with slightly different mean wingbeat frequencies (WBF, inset). The top histogram contains data from 1583 consecutive wingstrokes, and the lower histogram contains data from 206 consecutive wingstrokes.

View larger version (29K): [in a new window]   Fig. 7. Effects of stepwise deformation of the subalar membrane. (A) Tissue tension (red, right ordinate) and stretch receptor (SR) activity in response to square-wave steps in stretch (blue, left ordinate). In response to a rapid step in stretch, the stretch receptor produces a transient bout of high-frequency action potentials at the onset of the stretch, which declines rapidly to a tonic firing rate. (B) Time axis expansion of stretch receptor and tension responses illustrating that both stretch receptor firing rate and tension decay after the onset of a step in stretch (each plot was fitted with fractional power functions).

View larger version (12K): [in a new window]   Fig. 8. Stretch receptor (SR) responses to stepwise stretch for four moths (different symbols). (A) The stretch receptor response consists of an early high-frequency phasic burst, which rapidly decays to a sustained tonic discharge (50 ms bins, fitted to a fractional power function). (B) Firing rate during the early phasic response versus stretch amplitude (linear regression, r2=0.41; ANOVA, F=6.9, P=0.03). (C) Firing rate during the sustained tonic discharge versus stretch amplitude (linear regression, r2=0.8; ANOVA, F=32.6, P=0.0002).

View larger version (33K): [in a new window]   Fig. 9. Effects of deformation of the subalar membrane approximating in vivo conditions. Tension (red, right ordinate) and extracellular recording of stretch receptor activity (black) in response to sinusoidal stretch (blue, left ordinate) of the subalar membrane. Sample data are plotted for three oscillation frequencies indicated numerically within each plot.

View larger version (17K): [in a new window]   Fig. 10. Mean (N=4) stretch receptor (SR) responses to varying oscillation frequency and stretch amplitude. (A) Mean number of spikes per burst. (B) Mean stretch receptor firing rate (ANOVA, oscillation frequency, F=12.2, P=0.0012; amplitude, F=6.6, P=0.14). (C) Degree of stretch at the onset of the stretch receptor burst (ANOVA, oscillation frequency, F=9.9, P=0.0073). (D) Phase of stretch receptor burst with respect to peaks in the stretch waveform. The onset (termination) of a burst is indicated with filled (open) symbols. Different symbol shapes indicate the stretch amplitudes indicated numerically in B. Values are means ± S.D. Inset: data from D replotted as the difference in time (t) between peaks in stretch and onset (termination) of the burst indicated with filled (open) symbols