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1. The processing of proprioceptive signals in distributed networks: insights from insect motor control

   https://doi.org/10.1242/jeb.246182  

   Gebehart, Corinna; Büschges, Ansgar (January 2024, Journal of Experimental Biology)

   ABSTRACT The integration of sensory information is required to maintain body posture and to generate robust yet flexible locomotion through unpredictable environments. To anticipate required adaptations in limb posture and enable compensation of sudden perturbations, an animal's nervous system assembles external (exteroception) and internal (proprioception) cues. Coherent neuronal representations of the proprioceptive context of the body and the appendages arise from the concerted action of multiple sense organs monitoring body kinetics and kinematics. This multimodal proprioceptive information, together with exteroceptive signals and brain-derived descending motor commands, converges onto premotor networks – i.e. the local neuronal circuitry controlling motor output and movements – within the ventral nerve cord (VNC), the insect equivalent of the vertebrate spinal cord. This Review summarizes existing knowledge and recent advances in understanding how local premotor networks in the VNC use convergent information to generate contextually appropriate activity, focusing on the example of posture control. We compare the role and advantages of distributed sensory processing over dedicated neuronal pathways, and the challenges of multimodal integration in distributed networks. We discuss how the gain of distributed networks may be tuned to enable the behavioral repertoire of these systems, and argue that insect premotor networks might compensate for their limited neuronal population size by, in comparison to vertebrate networks, relying more heavily on the specificity of their connections. At a time in which connectomics and physiological recording techniques enable anatomical and functional circuit dissection at an unprecedented resolution, insect motor systems offer unique opportunities to identify the mechanisms underlying multimodal integration for flexible motor control. 

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2. Comparison of Proximal Leg Strain in Locomotor Model Organisms Using Robotic Legs

   Dinges, Gesa F; Zyhowski, William P; Goldsmith, C A; Szczecinski, Nicholas S (August 2023, Springer, Cham.)

   Insects use various sensory organs to monitor proprioceptive and exteroceptive information during walking. The measurement of forces in the exoskeleton is facilitated by campaniform sensilla (CS), which monitor resisted muscle forces through the detection of exoskeletal strains. CS are commonly found in leg segments arranged in fields, groups, or as single units. Most insects have the highest density of sensor locations on the trochanter, a proximal leg segment. CS are arranged homologously across species, suggesting comparable functions despite noted morphological differences. Furthermore, the trochanter–femur joint is mobile in some species and fused in others. To investigate how different morphological arrangements influence strain sensing in different insect species, we utilized two robotic models of the legs of the fruit fly Drosophila melanogaster and the stick insect Carausius morosus. Both insect species are past and present model organisms for unraveling aspects of motor control, thus providing extensive information on sensor morphology and, in-part, function. The robotic models were dynamically scaled to the legs of the insects, with strain gauges placed with correct orientations according to published data. Strains were detected during stepping on a treadmill, and the sensor locations and leg morphology played noticeable roles in the strains that were measured. Moreover, the sensor locations that were absent in one species relative to the other measured strains that were also being measured by the existing sensors. These findings contributed to our understanding of load sensing in animal locomotion and the relevance of sensory organ morphology in motor control. 

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3. Comparison of Proximal Leg Strain in Locomotor Model Organisms Using Robotic Legs

   Dinges, G.F.; Zyhowski, W.P.; Goldsmith, C.A.; Szczecinski, N.S. (August 2023, Biomimetic and Biohybrid Systems. Living Machines 2023.)

   Meder, F.; Hunt, A.; Margheri, L.; Mura, A.; Mazzolai, B. (Ed.)

   Insects use various sensory organs to monitor proprioceptive and exteroceptive information during walking. The measurement of forces in the exoskeleton is facilitated by campaniform sensilla (CS), which monitor resisted muscle forces through the detection of exoskeletal strains. CS are commonly found in leg segments arranged in fields, groups, or as single units. Most insects have the highest density of sensor locations on the trochanter, a proximal leg segment. CS are arranged homologously across species, suggesting comparable functions despite noted morphological differences. Furthermore, the trochanter–femur joint is mobile in some species and fused in others. To investigate how different morphological arrangements influence strain sensing in different insect species, we utilized two robotic models of the legs of the fruit fly Drosophila melanogaster and the stick insect Carausius morosus. Both insect species are past and present model organisms for unraveling aspects of motor control, thus providing extensive information on sensor morphology and, in-part, function. The robotic models were dynamically scaled to the legs of the insects, with strain gauges placed with correct orientations according to published data. Strains were detected during stepping on a treadmill, and the sensor locations and leg morphology played noticeable roles in the strains that were measured. Moreover, the sensor locations that were absent in one species relative to the other measured strains that were also being measured by the existing sensors. These findings contributed to our understanding of load sensing in animal locomotion and the relevance of sensory organ morphology in motor control. 

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4. Inhibition of knee joint sensory afferents alters covariation across strides between quadriceps muscles during locomotion

   https://doi.org/10.1152/japplphysiol.00591.2022  

   Alessandro, Cristiano; Prashara, Adarsh; Tentler, David P.; Tresch, Matthew C. (April 2023, Journal of Applied Physiology)

   Sport-related injuries to articular structures often alter the sensory information conveyed by joint structures to the nervous system. However, the role of joint sensory afferents in motor control is still unclear. Here, we evaluate the role of knee joint sensory afferents in the control of quadriceps muscles, hypothesizing that such sensory information modulates control strategies that limit patellofemoreal joint loading. We compared locomotor kinematics and muscle activity before and after inhibition of knee sensory afferents by injection of lidocaine into the knee capsule of rats. We evaluated whether this inhibition reduced the strength of correlation between the activity of vastus medialis (VM) and vastus lateralis (VL) both across strides and within each stride, coordination patterns that limit net mediolateral patellofemoral forces. We also evaluated whether this inhibition altered correlations among the other quadriceps muscle activity, the time-profiles of individual EMG envelopes, or movement kinematics. Neither the EMG envelopes nor limb kinematics was affected by the inhibition of knee sensory afferents. This perturbation also did not affect the correlations between VM and VL, suggesting that the regulation of patellofemoral joint loading is mediated by different mechanisms. However, inhibition of knee sensory afferents caused a significant reduction in the correlation between vastus intermedius (VI) and both VM and VL across, but not within, strides. Knee joint sensory afferents may therefore modulate the coordination between the vasti muscles but only at coarse time scales. Injuries compromising joint afferents might result in altered muscle coordination, potentially leading to persistent internal joint stresses and strains. NEW & NOTEWORTHY Sensory afferents originating from knee joint receptors provide the nervous system with information about the internal state of the joint. In this study, we show that these sensory signals are used to modulate the covariations among the activity of a subset of vasti muscles across strides of locomotion. Sport-related injuries that damage joint receptors may therefore compromise these mechanisms of muscle coordination, potentially leading to persistent internal joint stresses and strains. 

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5. Integration of feedforward and feedback control in the neuromechanics of vertebrate locomotion: a review of experimental, simulation and robotic studies

   https://doi.org/10.1242/jeb.245784  

   Ijspeert, Auke J.; Daley, Monica A. (August 2023, Journal of Experimental Biology)

   ABSTRACT Animal locomotion is the result of complex and multi-layered interactions between the nervous system, the musculo-skeletal system and the environment. Decoding the underlying mechanisms requires an integrative approach. Comparative experimental biology has allowed researchers to study the underlying components and some of their interactions across diverse animals. These studies have shown that locomotor neural circuits are distributed in the spinal cord, the midbrain and higher brain regions in vertebrates. The spinal cord plays a key role in locomotor control because it contains central pattern generators (CPGs) – systems of coupled neuronal oscillators that provide coordinated rhythmic control of muscle activation that can be viewed as feedforward controllers – and multiple reflex loops that provide feedback mechanisms. These circuits are activated and modulated by descending pathways from the brain. The relative contributions of CPGs, feedback loops and descending modulation, and how these vary between species and locomotor conditions, remain poorly understood. Robots and neuromechanical simulations can complement experimental approaches by testing specific hypotheses and performing what-if scenarios. This Review will give an overview of key knowledge gained from comparative vertebrate experiments, and insights obtained from neuromechanical simulations and robotic approaches. We suggest that the roles of CPGs, feedback loops and descending modulation vary among animals depending on body size, intrinsic mechanical stability, time required to reach locomotor maturity and speed effects. We also hypothesize that distal joints rely more on feedback control compared with proximal joints. Finally, we highlight important opportunities to address fundamental biological questions through continued collaboration between experimentalists and engineers. 

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