Temporal Differences between Load and Movement Signal Integration in the Sensorimotor Network of an Insect Leg

2021 ◽  
Author(s):  
Corinna Gebehart ◽  
Ansgar Büschges
Keyword(s):  
Motor Neurons ◽  
Stick Insect ◽  
Feedback Signal ◽  
Chordotonal Organ ◽  
Signal Integration ◽  
Sensory Stimuli ◽  
Temporal Differences ◽  
Sensorimotor Network ◽  
Load Sensing ◽  
And Function

Nervous systems face a torrent of sensory inputs, including proprioceptive feedback. Signal integration depends on spatially and temporally coinciding signals. It is unclear how relative time delays affect multimodal signal integration from spatially distant sense organs. We measured transmission times and latencies along all processing stages of sensorimotor pathways in the stick insect leg muscle control system using intra- and extracellular recordings. Transmission times of signals from load-sensing tibial and trochanterofemoral campaniform sensilla (tiCS, tr/fCS) to the premotor network were longer than from the movement-sensing femoral chordotonal organ (fCO). We characterized connectivity patterns from tiCS, tr/fCS, and fCO afferents to identified premotor nonspiking interneurons (NSIs) and motor neurons (MNs) by distinguishing short- and long-latency responses to sensory stimuli. Functional NSI connectivity depended on sensory context. The timeline of concurrent tiCS and fCO signals had an early phase of movement signal influences and delayed load influences. Temporal differences persisted into MN activity and muscle force development. We demonstrate a temporal difference in the processing of two distinct sensory modalities generated by the sensorimotor network and affecting motor output. The reported temporal differences in sensory processing and signal integration improve our understanding of sensory network computation and function in motor control.

Connections between thoraco-coxal proprioceptive afferents and motor neurons in the locust

2000 ◽  
Vol 203 (3) ◽  
pp. 435-445
Author(s):  
M. Wildman
Keyword(s):  
Electrical Stimulation ◽  
Sensory Neurons ◽  
Motor Neurons ◽  
Chordotonal Organ ◽  
Synaptic Connections ◽  
Afferent Neurons ◽  
Postsynaptic Potentials ◽  
The Common ◽  
Proprioceptive Afferents ◽  
Stimulation Of

The position of the coxal segment of the locust hind leg relative to the thorax is monitored by a variety of proprioceptors, including three chordotonal organs and a myochordotonal organ. The sensory neurons of two of these proprioceptors, the posterior joint chordotonal organ (pjCO) and the myochordotonal organ (MCO), have axons in the purely sensory metathoracic nerve 2C (N2C). The connections made by these afferents with metathoracic motor neurons innervating thoraco-coxal and wing muscles were investigated by electrical stimulation of N2C and by matching postsynaptic potentials in motor neurons with afferent spikes in N2C. Stretch applied to the anterior rotator muscle of the coxa (M121), with which the MCO is associated, evoked sensory spikes in N2C. Some of the MCO afferent neurons make direct excitatory chemical synaptic connections with motor neurons innervating the thoraco-coxal muscles M121, M126 and M125. Parallel polysynaptic pathways via unidentified interneurons also exist between MCO afferents and these motor neurons. Connections with the common inhibitor 1 neuron and motor neurons innervating the thoraco-coxal muscles M123/4 and wing muscles M113 and M127 are polysynaptic. Afferents of the pjCO also make polysynaptic connections with motor neurons innervating thoraco-coxal and wing muscles, but no evidence for monosynaptic pathways was found.

Intersegmental Coordination of Walking Movements in Stick Insects

2005 ◽  
Vol 93 (3) ◽  
pp. 1255-1265 ◽  
Author(s):  
Björn Ch. Ludwar ◽  
Marie L. Göritz ◽  
Joachim Schmidt
Keyword(s):  
Motor Pattern ◽  
Central Pattern Generators ◽  
Stick Insect ◽  
Neural Mechanisms ◽  
Chordotonal Organ ◽  
Adjacent Segment ◽  
Body Segments ◽  
Stick Insects ◽  
Pattern Generators ◽  
Leg Movements

Locomotion requires the coordination of movements across body segments, which in walking animals is expressed as gaits. We studied the underlying neural mechanisms of this coordination in a semi-intact walking preparation of the stick insect Carausius morosus. During walking of a single front leg on a treadmill, leg motoneuron (MN) activity tonically increased and became rhythmically modulated in the ipsilateral deafferented and deefferented mesothoracic (middle leg) ganglion. The pattern of modulation was correlated with the front leg cycle and specific for a given MN pool, although it was not consistent with functional leg movements for all MN pools. In an isolated preparation of a pair of ganglia, where one ganglion was made rhythmically active by application of pilocarpine, we found no evidence for coupling between segmental central pattern generators (CPGs) that could account for the modulation of MN activity observed in the semi-intact walking preparation. However, a third preparation provided evidence that signals from the front leg's femoral chordotonal organ (fCO) influenced activity of ipsilateral MNs in the adjacent mesothoracic ganglion. These intersegmental signals could be partially responsible for the observed MN activity modulation during front leg walking. While afferent signals from a single walking front leg modulate the activity of MNs in the adjacent segment, additional afferent signals, local or from contralateral or posterior legs, might be necessary to produce the functional motor pattern observed in freely walking animals.

scholarly journals Diminished ventral oligodendrocyte precursor generation results in the subsequent over-production of dorsal oligodendrocyte precursors of aberrant morphology and function

2020 ◽  
Author(s):  
Lev Starikov ◽  
Andreas H. Kottmann
Keyword(s):  
Spinal Cord ◽  
Motor Neurons ◽  
Ventricular Zone ◽  
Normal Numbers ◽  
Spinal Cord Development ◽  
Oligodendrocyte Precursor ◽  
And Function ◽  
Sod1 Mouse ◽  
Lateral Sclerosis ◽  
Ventral Spinal Cord

AbstractOligodendrocyte precursor cells (OPCs) arise sequentially first from a ventral and then from a dorsal precursor domain at the end of neurogenesis during spinal cord development. Whether the sequential production of OPCs is of physiological significance has not been examined. Here we show that ablating Shh signaling from nascent ventricular zone derivatives and partially from the floor plate results in a severe diminishment of ventral derived OPCs but normal numbers of motor neurons in the postnatal spinal cord. In the absence of ventral vOPCs, dorsal dOPCs populate the entire spinal cord resulting in an increased OPC density in the ventral horns. These OPCs take on an altered morphology, do not participate in the removal of excitatory vGlut1 synapses from injured motor neurons, and exhibit morphological features similar to those found in the vicinity of motor neurons in the SOD1 mouse model of Amyotrophic Lateral Sclerosis (ALS). Our data indicates that vOPCs prevent dOPCs from invading ventral spinal cord laminae and suggests that vOPCs have a unique ability to communicate with injured motor neurons.

scholarly journals Body side-specific changes in sensorimotor processing of movement feedback in a walking insect

2019 ◽  
Vol 122 (5) ◽  
pp. 2173-2186 ◽  
Author(s):  
Joscha Schmitz ◽  
Matthias Gruhn ◽  
Ansgar Büschges
Keyword(s):  
Stick Insect ◽  
The Body ◽  
Motor Output ◽  
Chordotonal Organ ◽  
Stimulus Velocity ◽  
Motor Processing ◽  
Sensorimotor Processing ◽  
Body Side ◽  
The Difference ◽  
Leg Kinematics

Feedback from load and movement sensors can modify timing and magnitude of the motor output in the stepping stick insect. One source of feedback is stretch reception by the femoral chordotonal organ (fCO), which encodes such parameters as the femorotibial (FTi) joint angle, the angular velocity, and its acceleration. Stimulation of the fCO causes a postural resistance reflex, during quiescence, and can elicit the opposite, so-called active reaction (AR), which assists ongoing flexion during active movements. In the present study, we investigated the role of fCO feedback for the difference in likelihood of generating ARs on the inside vs. the outside during curve stepping. We analyzed the effects of fCO stimulation on the motor output to the FTi and the neighboring coxa-trochanter and thorax-coxa joints of the middle leg. In inside and outside turns, the probability for ARs increases with increasing starting angle and decreasing stimulus velocity; furthermore, it is independent of the total angular excursion. However, the transition between stance and swing motor activity always occurs after a specific angular excursion, independent of the turning direction. Feedback from the fCO also has an excitatory influence on levator trochanteris motoneurons (MNs) during inside and outside turns, whereas the same feedback affects protractor coxae MNs only during outside steps. Our results suggest joint- and body side-dependent processing of fCO feedback. A shift in gain may be responsible for different AR probabilities between inside and outside turning, whereas the general control mechanism for ARs is unchanged. NEW & NOTEWORTHY We show that parameters of movement feedback from the tibia in an insect during curve walking are processed in a body side-specific manner, and how. From our results it is highly conceivable that the difference in motor response to the feedback supports the body side-specific leg kinematics during turning. Future studies will need to determine the source for the inputs that determine the local changes in sensory-motor processing.

scholarly journals Descending octopaminergic neurons modulate sensory-evoked activity of thoracic motor neurons in stick insects

2019 ◽  
Vol 122 (6) ◽  
pp. 2388-2413 ◽  
Author(s):  
Thomas Stolz ◽  
Max Diesner ◽  
Susanne Neupert ◽  
Martin E. Hess ◽  
Estefania Delgado-Betancourt ◽  
...  
Keyword(s):  
Motor Neurons ◽  
Stick Insect ◽  
Neuron Activity ◽  
Sense Organs ◽  
Descending Neurons ◽  
Walking Activity ◽  
Stick Insects ◽  
Evoked Activity ◽  
Sensory Evoked ◽  
Stimulation Of

Neuromodulatory neurons located in the brain can influence activity in locomotor networks residing in the spinal cord or ventral nerve cords of invertebrates. How inputs to and outputs of neuromodulatory descending neurons affect walking activity is largely unknown. With the use of matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and immunohistochemistry, we show that a population of dorsal unpaired median (DUM) neurons descending from the gnathal ganglion to thoracic ganglia of the stick insect Carausius morosus contains the neuromodulatory amine octopamine. These neurons receive excitatory input coupled to the legs’ stance phases during treadmill walking. Inputs did not result from connections with thoracic central pattern-generating networks, but, instead, most are derived from leg load sensors. In excitatory and inhibitory retractor coxae motor neurons, spike activity in the descending DUM (desDUM) neurons increased depolarizing reflexlike responses to stimulation of leg load sensors. In these motor neurons, descending octopaminergic neurons apparently functioned as components of a positive feedback network mainly driven by load-detecting sense organs. Reflexlike responses in excitatory extensor tibiae motor neurons evoked by stimulations of a femur-tibia movement sensor either are increased or decreased or were not affected by the activity of the descending neurons, indicating different functions of desDUM neurons. The increase in motor neuron activity is often accompanied by a reflex reversal, which is characteristic for actively moving animals. Our findings indicate that some descending octopaminergic neurons can facilitate motor activity during walking and support a sensory-motor state necessary for active leg movements. NEW & NOTEWORTHY We investigated the role of descending octopaminergic neurons in the gnathal ganglion of stick insects. The neurons become active during walking, mainly triggered by input from load sensors in the legs rather than pattern-generating networks. This report provides novel evidence that octopamine released by descending neurons on stimulation of leg sense organs contributes to the modulation of leg sensory-evoked activity in a leg motor control system.

scholarly journals Tenectin recruits integrin to stabilize bouton architecture and regulate vesicle release at the Drosophila neuromuscular junction

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Qi Wang ◽  
Tae Hee Han ◽  
Peter Nguyen ◽  
Michal Jarnik ◽  
Mihaela Serpe
Keyword(s):  
Neuromuscular Junction ◽  
Motor Neurons ◽  
Synaptic Cleft ◽  
Membrane Skeleton ◽  
Biologically Active ◽  
Striated Muscles ◽  
Local Engagement ◽  
Synaptic Junctions ◽  
Synaptic Boutons ◽  
And Function

Assembly, maintenance and function of synaptic junctions depend on extracellular matrix (ECM) proteins and their receptors. Here we report that Tenectin (Tnc), a Mucin-type protein with RGD motifs, is an ECM component required for the structural and functional integrity of synaptic specializations at the neuromuscular junction (NMJ) in Drosophila. Using genetics, biochemistry, electrophysiology, histology and electron microscopy, we show that Tnc is secreted from motor neurons and striated muscles and accumulates in the synaptic cleft. Tnc selectively recruits αPS2/βPS integrin at synaptic terminals, but only the cis Tnc/integrin complexes appear to be biologically active. These complexes have distinct pre- and postsynaptic functions, mediated at least in part through the local engagement of the spectrin-based membrane skeleton: the presynaptic complexes control neurotransmitter release, while postsynaptic complexes ensure the size and architectural integrity of synaptic boutons. Our study reveals an unprecedented role for integrin in the synaptic recruitment of spectrin-based membrane skeleton.

Load Signals Assist the Generation of Movement-Dependent Reflex Reversal in the Femur–Tibia Joint of Stick Insects

2006 ◽  
Vol 96 (6) ◽  
pp. 3532-3537 ◽  
Author(s):  
Turgay Akay ◽  
Ansgar Büschges
Keyword(s):  
Time Course ◽  
Stick Insect ◽  
Motor Output ◽  
Chordotonal Organ ◽  
Frequency Of Occurrence ◽  
Stick Insects ◽  
Extensor Motoneuron ◽  
Motoneuron Activity ◽  
First Time ◽  
Stimulation Of

Reinforcement of movement is an important mechanism by which sensory feedback contributes to motor control for walking. We investigate how sensory signals from movement and load sensors interact in controlling the motor output of the stick insect femur–tibia (FT) joint. In stick insects, flexion signals from the femoral chordotonal organ (fCO) at the FT joint and load signals from the femoral campaniform sensilla (fCS) are known to individually reinforce stance-phase motor output of the FT joint by promoting flexor and inhibiting extensor motoneuron activity. We quantitatively compared the time course of inactivation in extensor tibiae motoneurons in response to selective stimulation of fCS and fCO. Stimulation of either sensor generates extensor activity in a qualitatively similar manner but with a significantly different time course and frequency of occurrence. Inactivation of extensor motoneurons arising from fCS stimulation was more reliable but more than threefold slower compared with the extensor inactivation in response to flexion signals from the fCO. In contrast, simultaneous stimulation of both sense organs produced inactivation in motoneurons with a time course typical for fCO stimulation alone, but with a frequency of occurrence characteristic for fCS stimulation. This increase in probability of occurrence was also accompanied by a delayed reactivation of the extensor motoneurons. Our results indicate for the first time that load signals from the leg affect the processing of movement-related feedback in controlling motor output.

Multimodal Convergence of Presynaptic Afferent Inhibition in Insect Proprioceptors

1999 ◽  
Vol 82 (1) ◽  
pp. 512-514 ◽  
Author(s):  
Wolfgang Stein ◽  
Josef Schmitz
Keyword(s):  
Presynaptic Inhibition ◽  
Sensory Information ◽  
Reversal Potential ◽  
Stick Insect ◽  
Chordotonal Organ ◽  
Primary Afferent Depolarization ◽  
Campaniform Sensilla ◽  
Sense Organs ◽  
Position Sensitive ◽  
Conductance Increase

In the leg motor system of insects, several proprioceptive sense organs provide the CNS with information about posture and movement. Within one sensory organ, presynaptic inhibition shapes the inflow of sensory information to the CNS. We show here that also different proprioceptive sense organs can exert a presynaptic inhibition on each other. The afferents of one leg proprioceptor in the stick insect, either the position-sensitive femoral chordotonal organ or the load-sensitive campaniform sensilla, receive a primary afferent depolarization (PAD) from two other leg proprioceptors, the campaniform sensilla and/or the coxal hairplate. The reversal potential of this PAD is about −59 mV, and the PAD is associated with a conductance increase. The properties of this presynaptic input support the hypothesis that this PAD acts as presynaptic inhibition. The PAD reduces the amplitude of afferent action potentials and thus likely also afferent transmitter release and synaptic efficacy. These findings imply that PAD mechanisms of arthropod proprioceptors might be as complex as in vertebrates.

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