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First published online March 12, 2009
Journal of Experimental Biology 212, 1021-1031 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.023507
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Movement encoding by a stretch receptor in the soft-bodied caterpillar, Manduca sexta

Michael A. Simon* and Barry A. Trimmer

Department of Biology, Tufts University, Medford, MA 02155, USA


Figure 1
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  		Fig. 1. Manduca sexta larvae used in these experiments. (A) Lateral view of M. sexta. The animal is composed of a head, three thoracic segments, seven abdominal segments and a terminal segment. The experiments described in the present study examine the stretch receptor organ (SRO) in the abdominal segments. (B) The dorsal lateral nerve (DNL) innervates dorsal musculature, as well as the longitudinal SRO, which attaches to the body wall and spans the entire segment. Adapted from a drawing of Hyalophora cecropia (Beckel, 1958Go), whose major anatomical features are identical to those of Manduca. (C) Recordings of SRO activity during repeated strain cycling derived from the kinematics of crawling. The upper trace shows the length of cuticle-bearing SRO, the lower trace shows DNL activity measured via an extracellular electrode. Representative sample.

 

Figure 2
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  		Fig. 2. Validation of Gaussian white noise (GWN) stimulus. (A) Stimulus was generated with desired cutoff frequency (fc) and then upsampled and filtered to prevent stretch receptor organ (SRO) damage. The upper trace is a sample stimulus as measured by the ergometer on two repeated outputs, labeled red and black. The lower traces are responses to the sample stimulus on two occasions. Note the repeatability of the response to stimulus. Scale bar=200 ms. (B) Frequency spectrum of stimuli at specific fc. (C) Histogram of arm position values in GWN. All three fc generate nearly identical position distributions. (D) Histogram of stretch velocity at fc.

 

Figure 3
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  		Fig. 3. Kinematics of crawling and strike behaviors. (A) Crawling by M. sexta on a dowel. (i) Four abdominal segments shown in lateral view, anterior to the left, dorsal-side up. White box shows the area visualized in (ii). Arrow A indicates anterior. (ii) Images of fourth abdominal segment during a single crawl, at 0.33 s intervals. The fourth segment is highlighted to illustrate segment compression and expansion during a crawl cycle. (iii) Segment length was calculated from the length of dorsal interior muscle during crawling (see Movie 1 in supplementary material for crawling animal with fluorescent markers). Segment stretch velocity was computed as time-averaged time-derivative of segment length. Representative sample. (B) Strike response to pinching on terminal segment. (i) Upon pinching, the animal swings its head either left or right to strike at the stimulus source. Segment boundaries were painted for identification. Example shown is of a strike away from the measured side. White box shows the area visualized in (ii). (ii) Images of fifth abdominal segment during a strike away from the measured side, in 100 ms intervals. Arrows indicate segment boundaries. (iii) Segment length was calculated as the linear distance between approximate stretch receptor organ (SRO) attachment points. Segment velocity was calculated as the time-averaged time-derivative of segment length. Length and velocity may exceed those shown due to an unknown level of muscle curvature during strike. Note the different time and velocity scales for the two different behaviors. Representative samples.

 

Figure 4
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  		Fig. 4. Stretch receptor organ (SRO) tonic output frequency increased with displacement. M. sexta dorsal hemisegment was slowly stretched to randomly chosen lengths and held in that position for 20 s. Tonic frequency was averaged over an approximately 10 s period following termination of phasic activity. N=6 animals, 202 observations, error bars represent standard error.

 

Figure 5
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  		Fig. 5. Stretch receptor organ (SRO) phasic output increased with stretch velocity. (A) Recording of stretch-and-hold stimulus. M. sexta dorsal hemisegment was stretched 1 mm about the rest point at various velocities and then held briefly. The top trace is SRO length as measured by an ergometer. The bottom trace is SRO activity, as detected by an extracellular electrode. Maximum phasic frequency was calculated from the shaded area, beginning shortly before the start of a stretch and ending shortly after the end of that stretch. Representative sample. (B) Mean maximum phasic frequency at various stretch velocities. Mean maximum phasic frequency was determined from the mean of at least 10 consecutive stretches, where the maximum instantaneous frequency during stretch was determined for each separate stretch. N=5 animals, 48 observations, error bars represent standard error.

 

Figure 6
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  		Fig. 6. Wiener kernels of stretch receptor organ (SRO) response to Gaussian white noise (GWN) are characteristic of a position–velocity sensor. Corresponding shapes of (A) first- and (B) second-order Wiener kernels from recordings of M. sexta SROs responding to GWN stimuli with cutoff frequency (fc)=12.5, 25 and 50 Hz. Amplitude represents normalized spikes mm–1 s–1 of lag. N=12 animals.

 

Figure 7
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  		Fig. 7. Tonic adaptation correlated more strongly with a change in stretch receptor organ (SRO) length rather than length itself. (A) Example of tonic adaptation. Following a slow (non-phasic activity-inducing) change in SRO length, tonic activity initially changed to reflect the new SRO length and then adapted in the opposite direction of the initial change. The black line overlying the red trace shows fit to adaptation. Scale bar=30 s. (B) Quality of fit as characterized by R2 values. Median R2 was 0.8. (C) The length of SRO had a significant effect on the level of tonic activity but not on the degree of adaptation. (D) A change in the length of SRO had a significant effect on tonic adaptation but not on the level of tonic activity. Neither length nor change in length had a significant effect on the decay time constant.

 

Figure 8
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  		Fig. 8. Span of stretch did not affect phasic output. (A) The endpoint of a stretch was held constant and the start-point was varied in order to see if the span of a stretch affected the phasic output. (B) The data represent the stretch receptor organ (SRO) mean maximum phasic frequency following stretch of the fourth abdominal hemisegment in fifth-instar second day M. sexta. In all cases, endpoint of stretch was held at 0.5 mm over the rest point, with the total span varied between 25% and 150% of the control span (1 mm). In all other respects, this method was identical to previous phasic stretch-and-hold experiments. N=3 animals, 40 observations, error bars represent standard error.

 

Figure 9
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  		Fig. 9. Stretch receptor organ (SRO) phasic output decreased with decreased endpoint length. (A) In this series of experiments, the span of stretch was held constant and the start- and endpoints of stretch were varied about the rest length of the SRO. (B) For a given endpoint level, the mean, maximum phasic frequency was determined from at least 10 stretches at a particular start-point/endpoint combination. This was tested with six stretch velocities: 2, 4, 8, 16, 32 and 64 mm s–1. N=5 animals, 672 observations, error bars represent standard error.

 

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© The Company of Biologists Ltd 2009