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1.
Curr Biol ; 34(4): 910-915.e2, 2024 02 26.
Artigo em Inglês | MEDLINE | ID: mdl-38307023

RESUMO

Rhythmic locomotor activity, such as flying, swimming, or walking, results from an interplay between higher-order centers in the central nervous system, which initiate, maintain, and modify task-specific motor activity, downstream central pattern-generating neural circuits (CPGs) that can generate a default rhythmic motor output, and, finally, feedback from sense organs that modify basic motor activity toward functionality.1,2,3 In this context, CPGs provide phasic synaptic drive to motor neurons (MNs) and thereby support the generation of rhythmic activity for locomotion. We analyzed the synaptic drive that the leg MNs supplying the three main leg joints receive from CPGs in pharmacologically activated and deafferented preparations of the stick insect (Carausius morosus). We show that premotor CPGs pattern the tonic activity of five of the six leg MN pools by phasic inhibitory synaptic drive. These are the antagonistic MN pools supplying the thoraco-coxal joint and the femur-tibial joint4,5 and the levator MN pool supplying the coxa-trochanteral (CTr) joint. In contrast, rhythmic activity of the depressor MN pool supplying the CTr joint was found to be primarily based on a phasic excitatory drive. This difference is likely related to the pivotal role of the depressor muscle in generating leg stance during any walking situation. Thus, our results provide evidence for qualitatively differing mechanisms to generate rhythmic activity between MN pools in the same locomotor system.


Assuntos
Insetos , Caminhada , Animais , Insetos/fisiologia , Caminhada/fisiologia , Locomoção/fisiologia , Neurônios Motores/fisiologia
2.
Front Physiol ; 13: 883858, 2022.
Artigo em Inglês | MEDLINE | ID: mdl-35600292

RESUMO

We have just started to understand the mechanisms underlying flexibility of motor programs among segmental neural networks that control each individual leg during walking in vertebrates and invertebrates. Here, we investigated the mechanisms underlying curve walking in the stick insect Carausius morosus during optomotor-induced turning. We wanted to know, whether the previously reported body-side specific changes in a two-front leg turning animal are also observed in the other thoracic leg segments. The motor activity of the three major leg joints showed three types of responses: 1) a context-dependent increase or decrease in motor neuron (MN) activity of the antagonistic MN pools of the thorax-coxa (ThC)-joint during inside and outside turns; 2) an activation of 1 MN pool with simultaneous cessation of the other, independent of the turning direction in the coxa-trochanteral (CTr)-joint; 3) a modification in the activity of both FTi-joint MN pools which depended on the turning direction in one, but not in the other thorax segment. By pharmacological activation of the meso- or metathoracic central pattern generating networks (CPG), we show that turning-related modifications in motor output involve changes to local CPG activity. The rhythmic activity in the MN pools of the ThC and CTr-joints was modified similarly to what was observed under control conditions in saline. Our results indicate that changes in meso- and metathoracic motor activity during curve walking are leg-joint- and thorax-segment-specific, can depend on the turning direction, and are mediated through changes in local CPG activity.

3.
Curr Biol ; 32(10): 2334-2340.e3, 2022 05 23.
Artigo em Inglês | MEDLINE | ID: mdl-35476937

RESUMO

Because of scaling issues, passive muscle and joint forces become increasingly important as limb size decreases.1-3 In some small limbs, passive forces can drive swing in locomotion,4,5 and antagonist passive torques help control limb swing velocity.6 In stance, minimizing antagonist muscle and joint passive forces could save energy. These considerations predict that, for small limbs, evolution would result in the angle range over which passive forces are too small to cause limb movement (called "resting-state range" in prior insect work4 and "area of neutral equilibrium" in physics and engineering) correlating with the limb's typical working range, usually that in locomotion. We measured the most protracted and retracted thorax-femur (ThF) angles of the pro- (front), meso- (middle), and metathoracic (hind) leg during stick insect (Carausius morosus) walks. This ThF working range differed in the three leg types, being more posterior in more posterior legs. In other experiments, we manually protracted or retracted the denervated front, middle, and hind legs. Upon release, passive forces moved the leg in the opposite direction (retraction or protraction) until it reached the most protracted or most retracted edge of the ThF resting-state range. The ThF resting-state angle ranges correlated with the leg-type working range, being more posterior in more posterior legs. The most protracted ThF walking angles were more retracted than the post-protraction ThF angles, and the most retracted ThF walking angles were similar to the post-retraction ThF angles. These correlations of ThF working- and resting-state ranges could simplify motor control and save energy. These data also provide an example of evolution altering behavior by changing passive muscle and joint properties.7.


Assuntos
Extremidades , Caminhada , Animais , Fenômenos Biomecânicos , Extremidades/fisiologia , Insetos/fisiologia , Locomoção/fisiologia , Extremidade Inferior/fisiologia , Torque
4.
Front Insect Sci ; 2: 818449, 2022.
Artigo em Inglês | MEDLINE | ID: mdl-38468811

RESUMO

The walking system of the stick insect is one of the most thoroughly described invertebrate systems. We know a lot about the role of sensory input in the control of stepping of a single leg. However, the neuronal organization and connectivity of the central neural networks underlying the rhythmic activation and coordination of leg muscles still remain elusive. It is assumed that these networks can couple in the absence of phasic sensory input due to the observation of spontaneous recurrent patterns (SRPs) of coordinated motor activity equivalent to fictive stepping-phase transitions. Here we sought to quantify the phase of motor activity within SRPs in the isolated and interconnected meso- and meta-thoracic ganglia. We show that SRPs occur not only in the meso-, but also in the metathoracic ganglia of the stick insect, discovering a qualitative difference between them. We construct a network based on neurophysiological data capable of reproducing the measured SRP phases to investigate this difference. By comparing network output to the biological measurements we confirm the plausibility of the architecture and provide a hypothesis to account for these qualitative differences. The neural architecture we present couples individual central pattern generators to reproduce the fictive stepping-phase transitions observed in deafferented stick insect preparations after pharmacological activation, providing insights into the neural architecture underlying coordinated locomotion.

5.
Curr Biol ; 31(9): R444-R445, 2021 05 10.
Artigo em Inglês | MEDLINE | ID: mdl-33974872

RESUMO

New research has shown that mechanosensitive neurons in the lateral spinal cord of the adult zebrafish sense lateral bending and inhibit both their rostrally-located counterparts and the central-rhythm-generating networks across the midline. The interplay of central and peripheral neural mechanisms has never been seen to be so tight.


Assuntos
Propriocepção , Peixe-Zebra , Animais , Neurônios , Medula Espinal , Proteínas de Peixe-Zebra
6.
Dev Neurobiol ; 80(1-2): 16-30, 2020 01.
Artigo em Inglês | MEDLINE | ID: mdl-32128970

RESUMO

Central pattern generators (CPGs) are neural circuits that based on their connectivity can generate rhythmic and patterned output in the absence of rhythmic external inputs. This property makes CPGs crucial elements in the generation of many kinds of rhythmic motor behaviors in insects, such as flying, walking, swimming, or crawling. Arguably representing the most diverse group of animals, insects utilize at least one of these types of locomotion during one stage of their ontogenesis. Insects have been extensively used to study the neural basis of rhythmic motor behaviors, and particularly the structure and operation of CPGs involved in locomotion. Here, we review insect locomotion with regard to flying, walking, and crawling, and we discuss the contribution of central pattern generation to these three forms of locomotion. In each case, we compare and contrast the topology and structure of the CPGs, and we point out how these factors are involved in the generation of the respective motor pattern. We focus on the importance of sensory information for establishing a functional motor output and we indicate behavior-specific adaptations. Furthermore, we report on the mechanisms underlying coordination between different body parts. Last but not least, by reviewing the state-of-the-art knowledge concerning the role of CPGs in insect locomotion, we endeavor to create a common ground, upon which future research in the field of motor control in insects can build.


Assuntos
Comportamento Animal/fisiologia , Geradores de Padrão Central/anatomia & histologia , Geradores de Padrão Central/fisiologia , Insetos/fisiologia , Locomoção/fisiologia , Animais
7.
PLoS One ; 14(8): e0220767, 2019.
Artigo em Inglês | MEDLINE | ID: mdl-31386699

RESUMO

Animal walking results from a complex interplay of central pattern generating networks (CPGs), local sensory signals expressing position, velocity and forces generated in the legs, and coordinating signals between neighboring legs. In particular, the CPGs control the activity of motoneuron (MN) pools which drive the muscles of the individual legs and are thereby responsible for the generation of rhythmic leg movements. The rhythmic activity of the CPGs as well as their connectivity can be modified by the aforementioned sensory signals. However, the precise nature of the interaction between the CPGs and these sensory signals has remained generally largely unknown. Experimental methods aiming at finding out details of these interactions often apply cholinergic agonists such as pilocarpine in order to induce rhythmic activity in the CPGs. Using this general approach, we removed the influence of sensory signals and investigated the putative connections between CPGs controlling the upward/downward movement in the different legs of the stick insect. The experimental data, i.e. the measured MN activities, underwent connectivity analysis using Dynamic Causal Modelling (DCM). This method can uncover the underlying coupling structure and strength between pairs of segmental CPGs. For the analysis we set up different coupling schemes (models) for DCM and compared them using Bayesian Model Selection (BMS). Models with contralateral connections in each segment and ipsilateral connections on both sides, as well as the coupling from the meta- to the ipsilateral prothoracic ganglion were preferred by BMS to all other types of models tested. Moreover, the intrasegmental coupling strength in the mesothoracic ganglion was the strongest and most stable in all three ganglia.


Assuntos
Extremidades/fisiologia , Gânglios dos Invertebrados/fisiologia , Rede Nervosa/fisiologia , Caminhada/fisiologia , Animais , Teorema de Bayes , Agonistas Colinérgicos , Insetos , Modelos Biológicos , Neurônios Motores/fisiologia
8.
PLoS One ; 13(8): e0202822, 2018.
Artigo em Inglês | MEDLINE | ID: mdl-30142206

RESUMO

The stick insect is a well-established experimental animal to study the neural basis of walking. Here, we introduce a preparation that allows combining calcium imaging in efferent neurons with electrophysiological recordings of motor neuron activity in the stick insect thoracic nerve cord. The intracellular free calcium concentration in middle leg retractor coxae motor neurons and modulatory octopaminergic DUM neurons was monitored after backfilling lateral nerve nl5 that contains the axons of these neurons with the calcium indicator Oregon Green BAPTA-1. Rhythmic spike activity in retractor and protractor motor neurons was evoked by pharmacological activation of central pattern generating neuronal networks and recorded extracellularly from lateral nerves. A primary goal of this study was to investigate whether changes in the intracellular free calcium concentration observed in motor neurons during oscillatory activity depend on action potentials. We show that rhythmic spike activity in leg motor neurons induced either pharmacologically or by tactile stimulation of the animal is accompanied by a synchronous modulation in the intracellular free calcium concentration. Calcium oscillations in motor neurons do not appear to depend on calcium influx through voltage-sensitive calcium channels that are gated by action potentials because Calcium oscillations persist after pharmacologically blocking action potentials in the motor neurons. Calcium oscillations were also apparent in the modulatory DUM neurons innervating the same leg muscle. However, the timing of calcium oscillations varied not only between DUM neurons and motor neurons, but also among different DUM neurons. Therefore, we conclude that the motor neurons and the different DUM neurons receive independent central drive.


Assuntos
Cálcio/metabolismo , Neurônios Eferentes/fisiologia , Animais , Potenciais Evocados/efeitos dos fármacos , Feminino , Insetos/fisiologia , Neurônios Motores/efeitos dos fármacos , Neurônios Motores/fisiologia , Neurônios Eferentes/efeitos dos fármacos , Neurônios Eferentes/enzimologia , Pilocarpina/farmacologia
9.
J Neurophysiol ; 118(4): 2296-2310, 2017 10 01.
Artigo em Inglês | MEDLINE | ID: mdl-28724783

RESUMO

To efficiently move around, animals need to coordinate their limbs. Proper, context-dependent coupling among the neural networks underlying leg movement is necessary for generating intersegmental coordination. In the slow-walking stick insect, local sensory information is very important for shaping coordination. However, central coupling mechanisms among segmental central pattern generators (CPGs) may also contribute to this. Here, we analyzed the interactions between contralateral networks that drive the depressor trochanteris muscle of the legs in both isolated and interconnected deafferented thoracic ganglia of the stick insect on application of pilocarpine, a muscarinic acetylcholine receptor agonist. Our results show that depressor CPG activity is only weakly coupled between all segments. Intrasegmental phase relationships differ between the three isolated ganglia, and they are modified and stabilized when ganglia are interconnected. However, the coordination patterns that emerge do not resemble those observed during walking. Our findings are in line with recent studies and highlight the influence of sensory input on coordination in slowly walking insects. Finally, as a direct interaction between depressor CPG networks and contralateral motoneurons could not be observed, we hypothesize that coupling is based on interactions at the level of CPG interneurons.NEW & NOTEWORTHY Maintaining functional interleg coordination is vitally important as animals locomote through changing environments. The relative importance of central mechanisms vs. sensory feedback in this process is not well understood. We analyzed coordination among the neural networks generating leg movements in stick insect preparations lacking phasic sensory feedback. Under these conditions, the networks governing different legs were only weakly coupled. In stick insect, central connections alone are thus insufficient to produce the leg coordination observed behaviorally.


Assuntos
Gânglios dos Invertebrados/fisiologia , Insetos/fisiologia , Interneurônios/fisiologia , Neurônios Motores/fisiologia , Agonistas Muscarínicos/farmacologia , Rede Nervosa/fisiologia , Caminhada/fisiologia , Animais , Feminino , Gânglios dos Invertebrados/efeitos dos fármacos , Insetos/efeitos dos fármacos , Interneurônios/efeitos dos fármacos , Neurônios Motores/efeitos dos fármacos , Rede Nervosa/efeitos dos fármacos , Pilocarpina/farmacologia
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