Slow Temporal Filtering May Largely Explain the Transformation of Stick Insect (Carausius morosus) Extensor Motor Neuron Activity Into Muscle Movement

Abstract

Understanding how nervous systems generate behavior requires understanding how muscles transform neural input into movement. The stick insect extensor tibiae muscle is an excellent system in which to study this issue because extensor motor neuron activity is highly variable during single leg walking and extensor muscles driven with this activity produce highly variable movements. We showed earlier that spike number, not frequency, codes for extensor amplitude during contraction rises, which implies the muscle acts as a slow filter on the time scale of burst interspike intervals (5–10 ms). We examine here muscle response to spiking variation over entire bursts, a time scale of hundreds of milliseconds, and directly measure muscle time constants. Muscle time constants differ during contraction and relaxation, and contraction time constants, although variable, are always extremely slow (200–700 ms). Models using these data show that extremely slow temporal filtering alone can explain much of the observed transform properties. This work also revealed an unexpected (to us) ability of slow filtering to transform steadily declining inputs into constant amplitude outputs. Examination of the effects of time constant variability on model output showed that variation within an SD primarily altered output amplitude, but variation across the entire range also altered contraction shape. These substantial changes suggest that understanding the basis of this variation is central to predicting extensor activity and that the animal could theoretically vary muscle time constant to match extensor response to changing behavioral need.

Activity Patterns and Timing of Muscle Activity in the Forward Walking and Backward Walking Stick InsectCarausius morosus

“…This finding can be explained with the muscle properties reported for stick insects and smaller animals in general Hooper et al 2007Hooper et al , 2009. With decreasing diameter of a given muscle, the forces needed to overcome the passive forces of its antagonist become so large that muscle activity has to start well before an observed movement that is caused by the muscle contraction ).…”

“…Recent work on stick insect muscles Hooper et al 2007Hooper et al , 2009) highlights the slow responses of these muscles to neural input and thus the importance of direct measurement of muscle activation in describing how neural activity generates behavior in this system. Our EMG recordings of the six main middle leg muscles showed that only the muscles controlling the thorax-coxa joint (protractor, retractor) had large changes in activity when stick insects reversed walking direction (Fig.…”

Neural Control of Unloaded Leg Posture and of Leg Swing in Stick Insect, Cockroach, and Mouse Differs from That in Larger Animals

“…6). The justification for performing these experiments was that, although mammals do have fast and slow skeletal muscle fibers, even the slowest of these are much faster than stick insect extensor and other slow invertebrate nonspiking muscles, which can take hundreds to thousands of milliseconds to reach steady-state contraction levels in response to tonic motor neuron firing at physiological spike frequencies (Morris and Hooper, 1997;Hooper et al, 2007b). As such, if the slow properties of C. morosus muscles gave rise to unusual motor control strategies, these should be clearly shown by comparing motor control in C. morosus and animals, such as mammals, with much more rapidly contracting muscles.…”

Slow motor neuron stimulation of locust skeletal muscle: model and measurement

“…In contrast, stimulation of SETi produces very small twitches, approximately 100 times smaller in magnitude than the response to FETi, that sum over a large number of pulses. In the presented results, in response to CFT stimulation of SETi a steady state force was often not reached after 20 input pulses and Hooper et al (2007b) report that slow muscles can take hundreds of spikes to achieve steady state. Further differences exist between the contraction times of the muscles, with the time course of contraction in response to SETi stimulation being around 1.5 times that in response to FETi stimulation.…”