Distributed processing on the basis of parallel and antagonistic pathways simulation of the femur-tibia control system in the stick insect

Abstract

In inactive stick insects, sensory information from the femoral chordotonal organ (fCO) about position and movement of the femur-tibia joint is transferred via local nonspiking interneurons onto extensor and flexor tibiae motoneurons. Information is processed by the interaction of antagonistic parallel pathways at two levels: (1) at the input side of the nonspiking interneurons and (2) at the input side of the motoneurons. We tested by a combination of physiological experiments and computer simulation whether the known network topology and the properties of its elements are sufficient to explain the generation of the motor output in response to passive joint movements, that is resistance reflexes. In reinvestigating the quantitative characteristics of interneuronal pathways we identified 10 distinct types of nonspiking interneurons. Synaptic inputs from fCO afferents onto these interneurons are direct excitatory and indirect inhibitory. These connections were investigated with respect to position and velocity signals from the fCO. The results were introduced in the network simulation. The motor output of the simulation has the same characteristics as the real system, even when particular types of interneurons were removed in the simulation and the real system.

Premotor Interneurons in the Local Control of Stepping Motor Output for the Stick Insect Single Middle Leg

“…However, in all experiments of this study, the elicited response to stimulation resembled closely the known response to specific fCO stimulation (cf. Büschges 1990; Sauer et al 1996;Stein and Sauer 1998) and not to the one Akay (2002) described for specific CS stimulation where all investigated E-NSIs were hyperpolarized and I-NSIs didn't react at all. Two types of E-NSIs, E2 and E3, are morphologically quite similar (Büschges 1990) and differ only little in the position dependency of their responses to fCO stimulation.…”

“…Two types of E-NSIs, E2 and E3, are morphologically quite similar (Büschges 1990) and differ only little in the position dependency of their responses to fCO stimulation. Unfortunately, the position dependency of E3 varies in magnitude in the semi-intact preparation (Büschges 1990;Sauer et al 1996), and thus these cells could not be differentiated. Consequently all NSIs that showed morphological properties of E2 or E3 were lumped together as E2/3 (cf.…”

“…Like I1 and I2, NSI I4 provides inhibitory synaptic drive onto extensor MNs. Furthermore, I4 provides excitatory synaptic drive to the inhibitory extensor MN CI 1 (Sauer et al 1996) and to flexor tibiae and depressor trochanteris MNs (Büschges 1995). Throughout the stepping sequence the membrane potential of I4 (N ϭ 2, n ϭ 33) depolarized tonically a little above RMP.…”

“…These observations bear up the "parliamentary principle" formulated by Bässler (1993b); a term he coined for the distributed processing along parallel premotor pathways in the stick insect locomotor system. Besides evidence from the stick insect, in which such processing has been shown to occur at various levels of sensorimotor processing in postural and movement control (Büschges 1990;Büschges and Schmitz 1991;Kittmann et al 1996;Sauer et al 1996;review in Bü schges et al 2000), the same way of neural processing, called "distributed processing", has been described in other motor systems (e.g., leech bending reflexes: reviewed in Kristan 2000;vertebrates: e.g., Osborne and Popelle 1992). In the stick insect, that means that there were types of NSIs that were activated (depolarized) during swing and others that were activated during stance, regardless of their classification as E-(excitatory) or I-(inhibitory) NSI.…”

Control of stepping velocity in a single insect leg during walking

“…the extensor MNs and the inhibitory synaptic drive to the antagonistic pool, e.g. the flexor MNs, and vice versa (Büschges & Schmitz 1991;Büschges 1995;Sauer et al 1996). In another orthopteran insect (i.e.…”