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      Neuronal Innervation of the Subgenual Organ Complex and the Tibial Campaniform Sensilla in the Stick Insect Midleg

      research-article
      Insects
      MDPI
      neurobiology, mechanoreceptors, neuroanatomy Sipyloidea sipylus, physiology

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          Abstract

          Mechanosensory organs in legs play are crucial receptors in the feedback control of walking and in the detection of substrate-borne vibrations. Stick insects serve as a model for the physiological role of chordotonal organs and campaniform sensilla. This study documents, by axonal tracing, the neural innervation of the complex chordotonal organs and groups of campaniform sensilla in the proximal tibia of the midleg in Sipyloidea sipylus. In total, 6 nerve branches innervate the different sensory structures, and the innervation pattern associates different sensilla types by their position. Sensilla on the anterior and posterior tibia are innervated from distinct nerve branches. In addition, the variation in innervation is studied for five anatomical branching points. The most common variation is the innervation of the subgenual organ sensilla by two nerve branches rather than a single one. The fusion of commonly separated nerve branches also occurred. However, a common innervation pattern can be demonstrated, which is found in >75% of preparations. The variation did not include crossings of nerves between the anterior and posterior side of the leg. The study corrects the innervation of the posterior subgenual organ reported previously. The sensory neuroanatomy and innervation pattern can guide further physiological studies of mechanoreceptor organs and allow evolutionary comparisons to related insect groups.

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          Most cited references59

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          Functional morphology of insect mechanoreceptors.

          T. A. Keil (1997)
          This paper reviews the structure and function of insect mechanoreceptors with respect to their cellular, subcellular, and cuticular organization. Four types are described and their function is discussed: 1, the bristles; 2, the trichobothria; 3, the campaniform sensilla; and 4, the scolopidia. Usually, bristles respond to touch, trichobothria to air currents and sound, campaniform sensilla to deformation of the cuticle, and scolopidia to stretch. Mechanoreceptors are composed of four cells: a bipolar sensory neuron, which is enveloped by the thecogen, the trichogen, and the tormogen cells. Apically, the neuron gives off a ciliary dendrite which is attached to the stimulus-transmitting cuticular structures. In types 1-3, the tip of the dendrite contains a highly organized cytoskeletal complex of microtubules, the "tubular body," which is connected to the dendritic membrane via short rods, the "membrane-integrated cones" (MICs). The dendritic membrane is attached to the cuticle via fine attachment fibers. The hair-type sensilla (types 1, 2) are constructed as first-order levers, which transmit deflection of the hair directly to the dendrite tip. In campaniform sensilla (type 3), there is a cuticular dome instead of a hair and the dendrite is stimulated by deformation of the cuticle. In these three types, a slight lateral compression of the dendrite tip is most probably the effective stimulus. In scolopidia, the dendritic membrane is most probably stimulated by stretch. On the subcellular level, connectors between the cytoskeleton, the dendritic membrane, and extracellular (cuticular) structures are present in all four types and are thought to be engaged in membrane depolarization.
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            Mechanosensation and Adaptive Motor Control in Insects.

            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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              Six-legged walking in insects: how CPGs, peripheral feedback, and descending signals generate coordinated and adaptive motor rhythms.

              Walking is a rhythmic locomotor behavior of legged animals, and its underlying mechanisms have been the subject of neurobiological research for more than 100 years. In this article, we review relevant historical aspects and contemporary studies in this field of research with a particular focus on the role of central pattern generating networks (CPGs) and their contribution to the generation of six-legged walking in insects. Aspects of importance are the generation of single-leg stepping, the generation of interleg coordination, and how descending signals influence walking. We first review how CPGs interact with sensory signals from the leg in the generation of leg stepping. Next, we summarize how these interactions are modified in the generation of motor flexibility for forward and backward walking, curve walking, and speed changes. We then review the present state of knowledge with regard to the role of CPGs in intersegmental coordination and how CPGs might be involved in mediating descending influences from the brain for the initiation, maintenance, modification, and cessation of the motor output for walking. Throughout, we aim to specifically address gaps in knowledge, and we describe potential future avenues and approaches, conceptual and methodological, with the latter emphasizing in particular options arising from the advent of neurogenetic approaches to this field of research and its combination with traditional approaches.
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                Author and article information

                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                04 January 2020
                January 2020
                : 11
                : 1
                : 40
                Affiliations
                AG Integrative Sensory Physiology, Institute for Animal Physiology, Justus-Liebig-Universität Gießen, Heinrich-Buff-Ring 26 (IFZ), 35392 Gießen, Germany; johannes.strauss@ 123456physzool.bio.uni-giessen.de ; Tel.: +49-641-99-35253
                Article
                insects-11-00040
                10.3390/insects11010040
                7022571
                31947968
                5543057d-b13e-462b-a4a9-1a6c04bd04c5
                © 2020 by the author.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 11 December 2019
                : 02 January 2020
                Categories
                Article

                neurobiology,mechanoreceptors,neuroanatomy sipyloidea sipylus,physiology

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