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This review discusses how the nervous system controls the complex body movements keeping animals up and running. In particular, we revisit how research in insects has shed light on motor control principles that govern movements across the animal kingdom. Starting with the organization and evolution of the insect nervous system, we discuss insights into the neuronal control of behaviors varying in complexity, including escape, flight, crawling, walking, grooming, and courtship. These behaviors share specific control features. For instance, central pattern-generating circuits (CPG), which reside in proximity to the motor neurons and muscles, support the generation of rhythmic motor activity. The number of CPGs involved depends on the complexity of the motor apparatus controlled, such as wing pairs for flight or six pairs of multisegmented legs for walking. The different control architectures are introduced with respect to their organization, topology, and operation. Sensory feedback plays a pivotal role in shaping CPG activity into a functional, well-coordinated motor output. The activity of motor circuits is orchestrated by descending neurons connecting the brain to the ventral nerve cord or spinal cord, which initiate, maintain, modulate, and terminate different actions. We therefore discuss the current understanding of descending control and the contributions of individual, command-like descending neurons and population codes. To highlight how insights in insects help discover fundamental motor control principles, we cross-reference findings from other animals, particularly vertebrates. In addition, we discuss methodological advances that enabled breakthroughs in motor control research, including neurogenetics and connectomics, and discuss key open questions.
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Comparative connectomics of the descending and ascending neurons of the Drosophila nervous system: stereotypy and sexual dimorphism
Abstract In most complex nervous systems there is a clear anatomical separation between the nerve cord, which contains most of the final motor outputs necessary for behaviour, and the brain. In insects, the neck connective is both a physical and information bottleneck connecting the brain and the ventral nerve cord (VNC, spinal cord analogue) and comprises diverse populations of descending (DN), ascending (AN) and sensory ascending neurons, which are crucial for sensorimotor signalling and control. Integrating three separate EM datasets, we now provide a complete connectomic description of the ascending and descending neurons of the female nervous system ofDrosophilaand compare them with neurons of the male nerve cord. Proofread neuronal reconstructions have been matched across hemispheres, datasets and sexes. Crucially, we have also matched 51% of DN cell types to light level data defining specific driver lines as well as classifying all ascending populations. We use these results to reveal the general architecture, tracts, neuropil innervation and connectivity of neck connective neurons. We observe connected chains of descending and ascending neurons spanning the neck, which may subserve motor sequences. We provide a complete description of sexually dimorphic DN and AN populations, with detailed analysis of circuits implicated in sex-related behaviours, including female ovipositor extrusion (DNp13), male courtship (DNa12/aSP22) and song production (AN hemilineage 08B). Our work represents the first EM-level circuit analyses spanning the entire central nervous system of an adult animal.
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- Award ID(s):
- 2014862
- PAR ID:
- 10623800
- Author(s) / Creator(s):
- ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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Cymbalyuk, Gennady S (Ed.)Stick insects respond to visual or tactile stimuli with whole-body turning or directed reach-to-grasp movements. Such sensory-induced turning and reaching behaviour requires interneurons to convey information from sensory neuropils of the head ganglia to motor neuropils of the thoracic ganglia. To date, descending interneurons are largely unknown in stick insects. In particular, it is unclear whether the special role of the front legs in sensory-induced turning and reaching has a neuroanatomical correlate in terms of descending interneuron numbers. Here, we describe the population of descending interneurons with somata in the brain or gnathal ganglion in the stick insectCarausius morosus, providing a first map of soma cluster counts and locations. By comparison of interneuron populations with projections to the pro- and mesothoracic ganglia, we then estimate the fraction of descending interneurons that terminate in the prothoracic ganglion. With regard to short-latency, touch-mediated reach-to-grasp movements, we also locate likely sites of synaptic interactions between antennal proprioceptive afferents to the deutocerebrum and gnathal ganglion with descending or ascending interneuron fibres. To this end, we combine fluorescent dye stainings of thoracic connectives with stainings of antennal hair field sensilla. Backfills of neck connectives revealed up to 410 descending interneuron somata (brain: 205 in 19 clusters; gnathal ganglion: 205). In comparison, backfills of the prothorax-mesothorax connectives stained only up to 173 somata (brain: 83 in 16 clusters; gnathal ganglion: 90), suggesting that up to 60% of all descending interneurons may terminate in the prothoracic ganglion (estimated upper bound). Double stainings of connectives and antennal hair field sensilla revealed that ascending or descending fibres arborise in close proximity of afferent terminals in the deutocerebrum and in the middle part of the gnathal ganglia. We conclude that two cephalothoracic pathways may convey cues about antennal movement and pointing direction to thoracic motor centres via two synapses only.more » « less
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Accepted Manuscript1.0
- Posted Content:
- https://doi.org/10.1101/2024.06.04.596633
