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Maturation of muscle properties and its hormonal control in an adult insect

Uwe Rose^1,*, Michael Ferber² and Reinhold Hustert²

¹ Abteilung Neurobiologie, Universität Ulm, Albert-Einstein-Allee 11, D-89069 Ulm, Germany and
² Institut für Zoologie und Anthropologie der Universität Göttingen, Berlinerstraße 28, D-37073 Göttingen, Germany

View larger version (76K): [in a new window]   Fig. 1. (A) Sketch of an ovipositing locust. Extension of the abdomen is achieved by unfolding the intersegmental membranes between the fourth and seventh segments (oviposition segments, shaded). (B) The internal anatomy of the fourth, fifth and sixth abdominal segment (AS4–AS6; the internal layer of muscle fibres is at the top of the figure). Longitudinal muscles are referred to as ventral (sternal) or dorsal (tergal) longitudinal muscles. During oviposition, these muscles must follow and tolerate the extension. A and B were adapted from Rose et al. (Rose et al., 2000). a–d and a,b designate part of the muscles M212 and M213, respectively; exp., expiratory; insp., inspiratory.

View larger version (23K): [in a new window]   Fig. 2. Contraction properties of longitudinal muscle M214 measured in females less than 5 days old and females more than 18 days old. (A) The length/twitch tension relationship revealed that only muscles from mature females (>18 days old) were able to tolerate extensive lengthening without breakage of fibres. At 8 mm muscle length, the fibres still generated approximately 30 % of maximum tension. The tension generation of muscle fibres from females less than 5 days old declined rapidly after reaching a maximum, and the fibres broke at 4 mm (indicated by an arrow). fl/fmax, muscle tension at a particular length normalized to maximum tension. (B) Passive tension rose more steeply in muscles from females less than 5 days old than in females more than 18 days old. Above 4.5 mm, passive tension reached a plateau in muscles of females more than 18 days old. (C) A comparison of maximum forces generated by different stimulation frequencies revealed significantly higher tension in muscles from females more than 18 days old compared with muscles from females less than 5 days old (P<0.05). TW, twitch. An asterisk indicates statistical significance (Mann–Whitney rank sum test, P<0.05). Values are means ± S.E.M. (D) Examples of twitch and 5 Hz contractions. Muscles from females less than 5 days old had shorter twitch durations (see also Table 1) and higher tetanus fusion frequencies than muscles from females more than 18 days old.

View larger version (37K): [in a new window]   Fig. 3. A comparison of the properties of muscle fibres (M214) from mature females (>18 days old) treated with precocene or precocene plus juvenile hormone (JH). (A) The length/twitch tension relationship, showing that longitudinal muscles from precocene-treated females were not able to tolerate a length exceeding 4.5 mm without breaking (arrow). At this length, approximately 20 % of maximum tension was generated. In contrast, muscles from females treated with precocene plus JH tolerated extensions up to 8 mm and above and still generated more than 30 % of maximum tension. fl/fmax, muscle tension at a particular length normalized to maximum tension. (B) The passive length/tension relationship revealed pronounced differences. Passive tension increased steeply in muscles from precocene-treated females, whereas muscles from females treated with precocene plus JH generally exerted a lower tension that increased more slowly. (C) The maximum tension generated by the two groups differed significantly (P<0.05). The tension generated by muscles from precocene-treated animals was approximately one-third of the tension generated by muscles from animals treated with precocene plus JH. TW, twitch. An asterisk indicates statistical significance (Mann–Whitney rank sum test, P<0.05). Values are means ± S.E.M. (D) A comparison of tetanus fusion frequencies revealed no consistent differences comparable with those in Fig. 2D. (E) To confirm that the corpora allata (CA) from animals injected with precocene plus JH were indeed affected by precocene, the CA from these females were compared with those of untreated females (Control). The diameter of the CA from treated females was approximately 30 % of that of control females.

View larger version (48K): [in a new window]   Fig. 4. A comparison of the cross-sectional area of longitudinal muscles 169 and 214 from female locusts at different stages of development. (A,B) Cross sections revealed a significant, but not dramatic, hypertrophy of M169 during reproductive development (left-hand panel, <5 days old versus >18 days old). To examine a possible role for juvenile hormone in the hypertrophy, muscles from precocene-treated animals were also compared. For M169, there was no significant reduction in cross-sectional area evident for females treated with precocene (A,B; >18 days old versus >18 days old, precocene-treated). Muscle 214 (A,B, right-hand panel) showed marked hypertrophy during maturation. The degree of hypertrophy was significantly decreased in females treated with precocene (B, right-hand panel >18 days old versus >18 days old, precocene-treated), although values were still considerably higher than those of females less than 5 days old. The lines in B indicate significant differences (P<0.05, ANOVA with Tukey test). The number of experiments is given in parentheses. Values are means + S.E.M.

View larger version (31K): [in a new window]   Fig. 5. Stimulus-evoked action potentials revealed by current-clamp recordings from denervated muscle fibres. The amount of current injected was adjusted for each preparation to just reach the threshold at which action potentials were generated. (A) In females less than 5 days old, action potentials were non-overshooting with a moderate afterhyperpolarisation (left-hand panel). Muscles from females more than 18 days old generated overshooting action potentials with a pronounced afterhyperpolarisation (centre panel, see also B). In contrast, action potentials generated by fibres from females more than 18 days old treated with precocene resembled those from females less than 5 days old. (B) Action potentials from A shown on an expanded time scale for comparison. The action potential width for muscles of females more than 18 days old was increased. This increase was consistently absent from females treated with precocene. (C) Current injection evoked action potentials in fibres of muscle 169. Potentials from females less than 5 days old were non-overshooting and were followed by a small afterhyperpolarisation (C, left-hand panel). When females attained maturity, action potentials were overshooting but had still a small afterhyperpolarisation (C, centre panel). The action potentials of females treated with precocene were larger in amplitude than those of females less than 5 days old but were still non-overshooting. The afterhyperpolarisation of all groups was comparable (C, right-hand panel). (D) Potentials from C shown on an expanded time scale. The action potential width of mature female (untreated) muscle was increased.

View larger version (17K): [in a new window]   Fig. 6. Characterisation of action potentials recorded from muscle 214 from mature females. (A) The application of tetrodotoxin (TTX) (0.5 µmol l–1) had no effect on the generation or the shape of the action potential. (B) Application of Cd2+ (50 µmol l–1) completely blocked action potentials. Even increasing the injected current (from 24 to 40 nA) was not effective in generating potentials when Cd2+ was present in the bath. After washing in normal saline (10 min), action potentials reappeared. (C) Nifedipine (50 µmol l–1), which is known to modulate L-type Ca2+ channels, blocked the generation of action potentials even when the amount of current was increased (from 27.5 to 49 nA). Washing with normal saline reversed the blocking effect of nifedipine. The examples shown in A, B, C are from two different preparations.

View larger version (23K): [in a new window]   Fig. 7. Contraction properties of longitudinal muscle 169 (from non-oviposition segments) from females less than 5 days old and females more than 18 days old. (A,B) The length/tension curves revealed no age-dependent differences. Muscle fibres were not able to tolerate extensions of more than 4–4.5 mm (arrows indicate breakage of muscle fibres). Only the passive tension (B) was slightly increased in muscles of females more than 18 days old. fl/fmax, muscle tension at a particular length normalized to maximum tension. (C) The maximum tension exerted by muscle 169 of females more than 18 days old was consistently higher than that of females less than 5 days old, although the difference was not significant (P>0.05; Mann–Whitney rank sum test). TW, twitch. Values are means + S.E.M. (D) No consistent difference was found with respect to contraction kinetics (see also Table 1).

View larger version (22K): [in a new window]   Fig. 8. Contraction properties of longitudinal muscle 214 measured in males less than 5 days old and males more than 18 days old. (A) The length/twitch tension curves of the two groups were comparable. Muscle fibres were not able to tolerate extensions of more than 4 mm (arrows). fl/fmax, muscle tension at a particular length normalized to maximum tension. (B) Passive tension increased steeply in both groups, starting at 1 mm length, but was consistently higher in mature males (>18 days old), although the difference was not significant (P>0.05; Mann–Whitney rank sum test). (C) The maximum tension generated by muscles from males more than 18 days old exceeded that of muscles of males less than 5 days old. However, the means were not statistically different (P>0.05; Mann–Whitney rank sum test). Values are means ± S.E.M. TW, twitch. (D) No differences were evident with regard to the speed of contraction (see also Table 1) or tetanus fusion frequency.