A Leg-Local Neural Mechanism Mediates the Decision to Search in Stick Insects

Abstract

In many animals, individual legs can either function independently, as in behaviors such as scratching or searching, or be used in coordinated patterns with other legs, as in walking or climbing. While the control of walking has been extensively investigated, the mechanisms mediating the behavioral choice to activate individual legs independently are poorly understood. We examined this issue in stick insects, in which each leg can independently produce a rhythmic searching motor pattern if it doesn't find a foothold [1-4]. We show here that one non-spiking interneuron, I4, controls searching behavior in individual legs. One I4 is present in each hemi-segment of the three thoracic ganglia [5, 6]. Search-inducing sensory input depolarizes I4. I4 activity was necessary and sufficient to initiate and maintain searching movements. When substrate contact was provided, I4 depolarization no longer induced searching. I4 therefore both integrates search-inducing sensory input and is gated out by other sensory input (substrate contact). Searching thus occurs only when it is behaviorally appropriate. I4 depolarization never elicited stepping. These data show that individual, locally activated neurons can mediate the behavioral choice to use individual legs independently. This mechanism may be particularly important in insects' front legs, which can function independently like vertebrate arms and hands [7]. Similar local command mechanisms that selectively activate the pattern generators controlling repeated functional units such as legs or body segments may be present in other systems.

Speed-dependent interplay between local pattern-generating activity and sensory signals during walking inDrosophila

“…The animal still seemed active although no stepping was observed in the intact legs. Simultaneously, the stump oscillated up and down, performing searching-like movements (Berg et al, 2015), indicating that local pattern-generating networks were active (Fig. S1).…”

“…the desert ant (Zollikofer, 1994;Wahl et al, 2015) or the cockroach Tu, 1990, 1991). Alternatively, stump oscillations might resemble searching movements which are suppressed when the leg is touching the ground (Berg et al, 2015). In the stump, i.e.…”

Invertebrate Neurobiology: Bridging the Gap with a Local Command Interneuron

“…A remarkable finding of the study by Berg et al [1] is the identification of a specific interneuron that alone is capable of driving the entire searching motor sequence. The authors undertook a painstaking intracellular analysis to delineate the interneuron(s) responsible for controlling searching movements.…”

“…However, the organization of the neural circuits controlling these exploratory movements has remained unclear. As reported recently in Current Biology, Berg et al [1] have tackled this issue using the stick insect as a model system.…”

“…In their fascinating new study, Berg et al [1] provide a clear-cut demonstration that a single identified interneuron controls the whole sequence of searching leg movements in the stick insect. The authors took advantage of the accessibility of the semi-intact preparation, in which single leg stepping and searching can be induced by tactile stimulation while simultaneously monitoring the leg kinematics and muscle activity.…”