Contributions of structure and innervation pattern of the stick insect extensor tibiae muscle to the filter characteristics of the muscle-joint system

Abstract

It is shown that the low-pass filter characteristics of the muscle­joint system of the femur­tibia joint of the stick insect Cuniculina impigra result from co-contraction of the extensor and flexor tibiae muscles. The most distal region of the extensor muscle, which contains a high percentage of slow muscle fibres, is involved in this co-contraction. This conclusion results from the following evidence. (1) Inertial and friction forces do not affect the characteristics of the low-pass filter of the muscle­joint system. (2) There is some co-contraction of the extensor and flexor muscles during sinusoidal stimulation of the femoral chordotonal organ at high stimulus frequencies. Both muscles generate tonic forces that increase with increasing stimulus frequency and also increase with time from the beginning of stimulation until a plateau is reached. (3) For the extensor muscle, this tonic force is produced by its most distal portion only. (4) Electrical stimulation of the common inhibitory motoneurone (CI1) reduces the tonic force generated in this most distal portion of the extensor muscle. Therefore, CI1 stimulation reduces the amplitude of tibial movement in response to sinusoidal stimulation of the femoral chordotonal organ at stimulus frequencies below 0.5 Hz (over this frequency range, the tibial movement amplitude is a function of the force amplitude produced by the whole extensor muscle and there is no co-contraction), but at chordotonal organ stimulus frequencies of 1 Hz and above, CI1 stimulation increases the tibial movement amplitude (in this case, movement amplitude is limited by the degree of co-contraction of the extensor and flexor muscles). With repeated chordotonal organ stimulation at higher stimulus frequencies, the tibial movement amplitude steadily decreases. This must be a consequence of increasing levels of co-contraction of the extensor and flexor muscles, since at low stimulus frequencies (no co-contraction) there is no reduction in movement amplitude during repeated stimulations. It is concluded that co-contraction of the extensor and flexor tibiae muscles prevents instability in the reflex loop in spite of the high gain necessary for the generation of catalepsy. Therefore, the mechanism described can be considered to be an adaptation to the ecological niche occupied by this animal. The contribution of the distal part of the extensor muscle to this system can be switched off by the CI1 during active movements.