The Role of Sensory Signals From the Insect Coxa-Trochanteral Joint in Controlling Motor Activity of the Femur-Tibia Joint

Abstract

Interjoint coordination in multi-jointed limbs is essential for the generation of functional locomotor patterns. Here we have focused on the role that sensory signals from the coxa-trochanteral (CT) joint play in patterning motoneuronal activity of the femur-tibia (FT) joint in the stick insect middle leg. This question is of interest because when the locomotor system is active, movement signals from the FT joint are known to contribute to patterning of activity of the central rhythm-generating networks governing the CT joint. We investigated the influence of femoral levation and depression on the activity of tibial motoneurons. When the locomotor system was active, levation of the femur often induced a decrease or inactivation of tibial extensor activity while flexor motoneurons were activated. Depression of the femur had no systematic influence on tibial motoneurons. Ablation experiments revealed that this interjoint influence was not mediated by signals from movement and/or position sensitive receptors at the CT joint, i.e., trochanteral hairplate, rhombal hairplate, or internal levator receptor organ. Instead the influence was initiated by sensory signals from a field of campaniform sensillae, situated on the proximal femur (fCS). Selective stimulation of these fCS produced barrages of inhibitory postsynaptic potentials (IPSPs) in tibial extensor motoneurons and activated tibial flexor motoneurons. During pharmacologically activated rhythmic activity of the otherwise isolated mesothoracic ganglion (pilocarpine, 5 x 10(-4) M), deafferented except for the CT joint, levation of the femur as well had an inhibitory influence on tibial extensor motoneurons. However, the influence of femoral levation on the rhythm generated was rather labile and only sometimes a reset of the rhythm was induced. In none of the preparations could entrainment of rhythmicity by femoral movement be achieved, suggesting that sensory signals from the CT joint only weakly affect central rhythm-generating networks of the FT joint. Finally, we analyzed the role of sensory signals from the fCS during walking by recording motoneuronal activity in the single middle leg preparation with fCS intact and after their removal. These experiments showed that fCS activity plays an important role in generating tibial motoneuron activity during the stance phase of walking.

Control of stepping velocity in a single insect leg during walking

“…There are different possibilities for how this second depolarization is generated. Previous investigations show that sensory signals from strain and movement sensors reinforce flexor MN activation during voluntary and locomotor movements (Bässler 1986;Akay et al 2001;summary in Bässler & Büschges 1998), as has been shown in a variety of walking systems (for summary, see Pearson 1993;Büschges & El Manira 1998). At present, it is not known what other sources of synaptic inputs are contributing to the control of flexor MN activity.…”

“…On the one hand, excitatory synaptic inputs are conceivable that are related to touch down of the leg, e.g. from tarsal receptors (Laurent & Hustert 1988) or campaniform sensilla on the leg (Newland & Emptage 1996;Akay et al 2001). However, on the other hand, some arguments point towards a different origin.…”

Proprioceptors involved in stinging response of the honeybee, Apis mellifera

“…These sensilla are arranged on various limbs of insects in groups with distinctive distributions, where cuticular strain is induced both by passive loading of the leg and during muscle-driven locomotion (Hofmann and Bässler, 1982;Hustert et al, 1981;Pringle, 1938;Spinola and Chapman, 1975). Sensory signals from the femoral and trochanteral campaniform sensilla affect the timing of the central pattern generator for insect walking, and have a primary role in coordinating movements of the distal leg joints (Akay et al, 2001(Akay et al, , 2004). …”

Segment Specificity of Load Signal Processing Depends on Walking Direction in the Stick Insect Leg Muscle Control System

“…To determine which of the trochantero-femoral load sensors were responsible for the transitions in bursting activities, we successively ablated the campaniform sensilla fields on the trochanter and femur, the trCS and fCS, respectively, in the single-legged preparations both at rest and during alternating coxal motoneurons activity (Bässler, 1977;Akay et al, 2001Akay et al, , 2004. Removal of the fCS (N ϭ 3) did not affect reflex activation of coxal motoneurons at rest (data not shown) or alter the initiation incidence of the most often detected changes in motor activity for a given CS stimuli (Fig.…”

“…Input from the CS fields of the trochantero-femur substantially alter leg motor output (Bässler, 1977;Schmitz, 1993;Schmitz and Stein, 2000;Akay et al, 2001Akay et al, , 2004 and help coordinate the motoneuron activities of the indi-vidual central pattern generating networks that control the different joints. The femoral CS afferents alter, in particular, the central rhythm generator (CRG) of the femur-tibia (FT) joint so as to promote and enhance flexor tibiae motoneuron activity during stance (Akay et al, 2001). Signals from the trochanteral CS (trCS), alternatively, change thorax-coxa (ThC) joint CRG activity (in forward walking) by promoting retractor coxae motoneuron activity during stance (Akay et al, 2004).…”