Christoph Guschlbauer

Neural control of unloaded leg posture and of leg swing in stick insect, cockroach, and mouse differs from that in larger animals.

Stick insect (Carausius morosus) leg muscles contract and relax slowly. Control of stick insect leg posture and movement could therefore differ from that in animals with faster muscles. Consistent with this possibility, stick insect legs maintained constant posture without leg motor nerve activity when the animals were rotated in air. That unloaded leg posture was an intrinsic property of the legs was confirmed by showing that isolated legs had constant, gravity-independent postures. Muscle ablation experiments, experiments showing that leg muscle passive forces were large compared with gravitational forces, and experiments showing that, at the rest postures, agonist and antagonist muscles generated equal forces indicated that these postures depended in part on leg muscles. Leg muscle recordings showed that stick insect swing motor neurons fired throughout the entirety of swing. To test whether these results were specific to stick insect, we repeated some of these experiments in cockroach (Periplaneta americana) and mouse. Isolated cockroach legs also had gravity-independent rest positions and mouse swing motor neurons also fired throughout the entirety of swing. These data differ from those in human and horse but not cat. These size-dependent variations in whether legs have constant, gravity-independent postures, in whether swing motor neurons fire throughout the entirety of swing, and calculations of how quickly passive muscle force would slow limb movement as limb size varies suggest that these differences may be caused by scaling. Limb size may thus be as great a determinant as phylogenetic position of unloaded limb motor control strategy.

The extensor tibiae muscle of the stick insect: biomechanical properties of an insect walking leg muscle

SUMMARY We investigated the properties of the extensor tibiae muscle of the stick insect (Carausius morosus) middle leg. Muscle geometry of the middle leg was compared to that of the front and hind legs and to the flexor tibiae, respectively. The mean length of the extensor tibiae fibres is 1.41±0.23 mm and flexor fibres are 2.11±0.30 mm long. The change of fibre length with joint angle was measured and closely follows a cosine function. Its amplitude gives effective moment arm lengths of 0.28±0.02 mm for the extensor and 0.56±0.04 mm for the flexor. Resting extensor tibiae muscle passive tonic force increased from 2 to 5 mN in the maximum femur–tibia (FT)-joint working range when stretched by ramps. Active muscle properties were measured with simultaneous activation (up to 200 pulses s–1) of all three motoneurons innervating the extensor tibiae, because this reflects most closely physiological muscle activation during leg swing. The force–length relationship corresponds closely to the typical characteristic according to the sliding filament hypothesis: it has a plateau at medium fibre lengths, declines nearly linearly in force at both longer and shorter fibre lengths, and the muscles working range lies in the short to medium fibre length range. Maximum contraction velocity showed a similar relationship. The force–velocity relationship was the traditional Hill curve hyperbola, but deviated from the hyperbolic shape in the region of maximum contraction force close to the isometric contraction. Step-like changes in muscle length induced by loaded release experiments characterised the non-linear series elasticity as a quadratic spring.

A neuromechanical model for the neuronal basis of curve walking in the stick insect.

The coordination of the movement of single and multiple limbs is essential for the generation of locomotion. Movement about single joints and the resulting stepping patterns are usually generated by the activity of antagonistic muscle pairs. In the stick insect, the three major muscle pairs of a leg are the protractor and retractor coxae, the levator and depressor trochanteris, and the flexor and extensor tibiae. The protractor and retractor move the coxa, and thereby the leg, forward and backward. The levator and depressor move the femur up and down. The flexor flexes, and the extensor extends the tibia about the femur-tibia joint. The underlying neuronal mechanisms for a forward stepping middle leg have been thoroughly investigated in experimental and theoretical studies. However, the details of the neuronal and mechanical mechanisms driving a stepping single leg in situations other than forward walking remain largely unknown. Here, we present a neuromechanical model of the coupled three joint control system of the stick insects middle leg. The model can generate forward, backward, or sideward stepping. Switching between them is achieved by changing only a few central signals controlling the neuromechanical model. In kinematic simulations, we are able to generate curve walking with two different mechanisms. In the first, the inner middle leg is switched from forward to sideward and in the second to backward stepping. Both are observed in the behaving animal, and in the model and animal alike, backward stepping of the inner middle leg produces tighter turns than sideward stepping.

Muscles: Non-linear Transformers of Motor Neuron Activity

Predicting movement from neural activity requires quantitative understanding of muscle response to motor neuron input. Muscles are sufficiently complicated that fulfilling this goal requires computer simulation. We therefore first explain in considerable detail one approach to modeling muscle. We then provide multiple examples of how muscle intrinsic properties and muscle diversity make straightforward predictions of how muscles transform neural input into movement impossible, including the dependence of muscle velocity on sarcomere number, the inadequacy of mean data in muscle modeling, the effects of muscle low-pass filtering, spike-number vs. spike frequency coding for contraction amplitude, how the role of passive muscle force in movement generation varies as a function of limb size, how muscles produce forces greater than their ‘maximum force’, energy conserving mechanisms, muscles that brake rather than produce movement, and how muscles can generate restoring responses (preflexes) to perturbing input in the absence of sensory feedback.