Directional specificity and encoding of muscle forces and loads by stick insect tibial campaniform sensilla, including receptors with round cuticular caps

Zill, Sasha N.; Chaudhry, Sumaiya; Büschges, Ansgar; Schmitz, Josef

doi:10.1016/j.asd.2013.10.001

Cited by 37 publications

(36 citation statements)

References 60 publications

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“…Another are force-and loadsensing campaniform sensilla, which respond only to resisted movements, as occur in standing to generate anti-gravity leg forces and in walking when descending legs contact the sub-strate. Consistent with this role, in walking, campaniform sensilla are active during stance [36], but not swing [37]. They are thus expected to be inactive during searches, in which substrate contact never occurs.…”

Section: Resultsmentioning

confidence: 83%

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

et al. 2015

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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.

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Section: Resultsmentioning

confidence: 83%

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

et al. 2015

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“…For example, campaniform sensilla on the stick insect trochanter are positioned to encode increases and decreases in mechanical load at the nearby leg joint [63]. Campaniform sensilla neurons are active when leg movements are resisted with a mechanical probe, but do not fire during unresisted leg movements, indicating that they encode mechanical load as resistance to muscle contraction [63, 64]. In this regard, the campaniform sensilla perform a function similar to that of vertebrate Golgi tendon organs [4].…”

Section: Insect Mechanoreceptorsmentioning

confidence: 99%

Mechanosensation and Adaptive Motor Control in Insects

2016

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Summary The ability of animals to flexibly navigate through complex environments depends on the integration of sensory information with motor commands. The sensory modality most tightly linked to motor control is mechanosensation. Adaptive motor control depends critically on an animal’s ability to respond to mechanical forces generated both within and outside the body. The compact neural circuits of insects provide appealing systems to investigate how mechanical cues guide locomotion in rugged environments. Here, we review our current understanding of mechanosensation in insects and its role in adaptive motor control. We first examine the detection and encoding of mechanical forces by primary mechanoreceptor neurons. We then discuss how central circuits integrate and transform mechanosensory information to guide locomotion. Because most studies in this field have been performed in locusts, cockroaches, crickets, and stick insects, the examples we cite here are drawn mainly from these ‘big insects’. However, we also pay particular attention to the tiny fruit fly, Drosophila, where new tools are creating new opportunities, particularly for understanding central circuits. Our aim is to show how studies of big insects have yielded fundamental insights relevant to mechanosensation in all animals, and also to point out how the Drosophila toolkit can contribute to future progress in understanding mechanosensory processing.

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“…Sensory structures distal to the lesion are absent and cannot provide information (see Bässler, 1983). Campaniform sensilla on the coxa and trochanter are probably silent because of missing ground contact; campaniform sensilla in insects are activated only when the leg is loaded or when movements are resisted (Zill et al, 2009(Zill et al, , 2011(Zill et al, , 2013. Consequently, most of the intra-leg sensory signals that are known to dominate motor output during walking can probably be ruled out as playing a role in oscillatory stump movements.…”

Section: Rhythmic Stump Activitymentioning

confidence: 99%

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

Berendes

Zill

Büschges

et al. 2016

Journal of Experimental Biology

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In insects, the coordinated motor output required for walking is based on the interaction between local pattern-generating networks providing basic rhythmicity and leg sensory signals, which modulate this output on a cycle-to-cycle basis. How this interplay changes speed-dependently and thereby gives rise to the different coordination patterns observed at different speeds is not sufficiently understood. Here, we used amputation to reduce sensory signals in single legs and decouple them mechanically during walking in Drosophila. This allowed for the dissociation between locally generated motor output in the stump and coordinating influences from intact legs. Leg stumps were still rhythmically active during walking. Although the oscillatory frequency in intact legs was dependent on walking speed, stumps showed a high and relatively constant oscillation frequency at all walking speeds. At low walking speeds we found no strict cycle-to-cycle coupling between stumps and intact legs. In contrast, at high walking speeds stump oscillations were strongly coupled to the movement of intact legs on a one-to-one basis. Although during slow walking there was no preferred phase between stumps and intact legs, we nevertheless found a preferred time interval between touch-down or lift-off events in intact legs and levation or depression of stumps. Based on these findings, we hypothesize that, as in other insects, walking speed in Drosophila is predominantly controlled by indirect mechanisms and that direct modulation of basic pattern-generating circuits plays a subsidiary role. Furthermore, interleg coordination strength seems to be speed-dependent and greater coordination is evident at higher walking speeds.

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Directional specificity and encoding of muscle forces and loads by stick insect tibial campaniform sensilla, including receptors with round cuticular caps

Cited by 37 publications

References 60 publications

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

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

Mechanosensation and Adaptive Motor Control in Insects

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

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