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 ◽  
...  

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.

2006 ◽  
Vol 96 (6) ◽  
pp. 3532-3537 ◽  
Author(s):  
Turgay Akay ◽  
Ansgar Büschges

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.


Author(s):  
Jens Peter Gabriel ◽  
Ansgar Büschges

In the single middle leg preparation of the stick insect walking on a treadmill, the activity of flexor and extensor tibiae motor neurons and muscles, which are responsible for the movement of the tibia in stance and swing phases, respectively, was investigated with respect to changes in stepping velocity. Changes in stepping velocity were correlated with cycle period. There was a close correlation of flexor motor neuron activity (stance phase) with stepping velocity, but the duration and activation of extensor motor neurons (swing phase) was not altered. The depolarization of flexor motor neurons showed two components. At all step velocities, a stereotypic initial depolarization was generated at the beginning of stance phase activity. A subsequent larger depolarization and activation was tightly linked to belt velocity, i.e. it occurred earlier and with larger amplitude during fast steps compared with slow steps. Alterations in a tonic background excitation appear not to play a role in controlling the motor neuron activity for changes in stepping velocity. Our results indicate that in the single insect leg during walking, mechanisms for altering stepping velocity become effective only during an already ongoing stance phase motor output. We discuss the putative mechanisms involved.


1992 ◽  
Vol 173 (1) ◽  
pp. 91-108 ◽  
Author(s):  
R. Kittmann ◽  
J. Schmitz

The femoral chordotonal organ (fCO), one of the largest proprioceptive sense organs in the leg of the stick insect, is important for the control of the femur-tibia joint during standing and walking. It consists of a ventral scoloparium with about 80 sensory cells and a dorsal scoloparium with about 420 sensory cells. The present study examines the function of these scoloparia in the femur-tibia control loop. Both scoloparia were stimulated independently and the responses in the extensor tibiae motoneurones were recorded extra- and intracellularly. The ventral scoloparium, which is the smaller of the two, functions as the transducer of the femur-tibia control loop. Its sensory cells can generate the known resistance reflexes. The dorsal scoloparium serves no function in the femur-tibia control loop and its stimulation elicited no or only minor reactions in the extensor motoneurones. A comparison with other insect leg proprioceptors shows that a morphological subdivision of these organs often indicates a functional specialization.


1989 ◽  
Vol 144 (1) ◽  
pp. 81-111 ◽  
Author(s):  
ANSGAR BÜSCHGES

The femoral chordotonal organ (ChO) of the right middle leg of the inactive stick insect Carausius morosus was stimulated by applying movements having a ramp-like time course, while recordings were made from local and interganglionic interneurones in the anterior ventral median part of the ganglion. Position, velocity and acceleration of the movements were varied independently and the interneurones were categorized on the basis of their responses to the changes in these parameters. Position-sensitivity was always accompanied by responses to velocity and/or acceleration. Velocity-sensitive responses were excitatory or inhibitory and were produced by elongation or relaxation, or by both. In some cases, velocity-sensitive neurones were also affected by position and acceleration. Acceleration responses were always excitatory and were often found in neurones that showed no effects of velocity or position. It is inferred that sensory input from different receptors in the ChO is processed by single interneurones. No interneurone in the recording region was found to be directly involved in the resistance reflex of the extensor tibiae motoneurones, elicited by stimulation of the ChO.


2000 ◽  
Vol 83 (6) ◽  
pp. 3337-3350 ◽  
Author(s):  
Andrew K. Tryba ◽  
Roy E. Ritzmann

In a previous study, we combined joint kinematics and electromyograms (EMGs) to examine the change in the phase relationship of two principal leg joints during walking and searching. In this study, we recorded intracellularly from motor neurons in semi-intact behaving animals to examine mechanisms coordinating extension at these leg joints. In particular, we examined the change in the phase of the coxa-trochanter (CTr) and femur-tibia (FT) joint extension during walking and searching. In doing so, we discovered marked similarities in the activity of CTr and FT joint extensor motor neurons at the onset of extension during searching and at the end of stance during walking. The data suggest that the same interneurons may be involved in coordinating the CTr and FT extensor motor neurons during walking and searching. Previous studies in stick insects have suggested that extensor motor neuron activity during the stance phase of walking results from an increase in tonic excitation of the neuron leading to spiking that is periodically interrupted by centrally generated inhibition. However, the CTr and FT extensor motor neuron activity during walking consists of characteristic phasic modulations in motor neuron frequency within each step cycle. The phasic increases and decreases in extensor EMG frequency during stance are associated with kinematic events (i.e., foot set-down and joint cycle transitions) during walking. Sensory feedback associated with these events might be responsible for phasic modulation of the extensor motor neuron frequency. However, our data rule out the possibility that sensory cues resulting from foot set-down are responsible for a decline in CTr extensor activity that is characteristic of the Blaberusstep cycle. Our data also suggest that both phasic excitation and inhibition contribute to extensor motor neuron activity during the stance phase of walking.


1996 ◽  
Vol 76 (1) ◽  
pp. 93-108 ◽  
Author(s):  
P. Skorupski

1. This paper investigates the effect of octopamine on spontaneous and reflex motor output of crayfish leg motor neurons. Octopamine modulated spontaneous activity, both rhythmic and tonic, and dramatically modulated the pattern of reflex motor output elicited by stimulating identified proprioceptors of the basal limb. 2. Spontaneous reciprocal motor patterns, involving alternating bursts of promotor and remotor motor neuron activity, were reversibly abolished by octopamine. The threshold concentration for this effect was approximately 1 microM. 3. At concentrations greater than approximately 10 microM octopamine inhibited spontaneous promotor nerve activity in both bursting and nonbursting preparations. In some experiments promotor inhibition was correlated with the induction of tonic remotor nerve activity. The EC50 for complete inhibition of promotor nerve activity by octopamine was 20-30 microM. 4. Reflexes mediated by two basal limb proprioceptors, the thoracocoxal muscle receptor organ (TCMRO; which signals leg promotion) and the thoracocoxal chordotonal organ (TCCO; which signals leg remotion) were analyzed in a number of promotor and remotor motor neurons. In both cases assistance reflexes (excitation of promotors by the TCCO and remotors by the TCMRO) were restricted to subgroups of the motor pool. Among remotor motor neurons, the first two units recruited during bursts of spontaneous activity were members of the assistance reflex group (group 1). A third unit, sometimes recruited during more intense spontaneous bursts, was excited by TCCO stimulation and was therefore a member of the resistance reflex group (group 2). Other resistance group remotors were also excited by the TCCO, but this input normally remained subthreshold. 5. Stimulation of the TCCO afferent nerve elicited excitatory postsynaptic potentials (EPSPs) in group 2 (resistance group) remotor motor neurons at a latency compatible with a monosynaptic connection. The same stimulation excited group 1 (assistance group) promotor motor neurons, but at a greater and more variable latency. Thus the remotor resistance reflex from the TCCO is probably monosynaptic, but the promotor assistance reflex, also elicited by TCCO stimulation, is likely to be di- or polysynaptic. Assistance group (group 1) remotor motor neurons are inhibited by mechanical stimulation of the TCCO, or electrical stimulation of its nerve. 6. Octopamine had selective effects on individual remotor units. First, assistance group remotor motor neurons were affected in two ways. One unit was inhibited, so that reflex spiking in response to TCMRO stimulation was abolished. A second unit was not inhibited, but its reflex response mode changed, so that instead of responding to TCMRO input with an assistance reflex, it responded to TCCO input with a resistance reflex. Second, among motor neurons that normally respond to TCCO input with resistance reflexes, these responses were enhanced by octopamine. 7. Promotor motor neurons were inhibited by octopamine and reflex responses were also affected selectively. Responses to TCCO input (assistance reflexes) were abolished; whereas, responses to TCMRO input (resistance reflexes) were relatively less affected. 8. Intracellular recordings revealed that the majority of remotor motor neurons depolarized in the presence of octopamine. In preparations where these could be classified on the basis of TCMRO/ TCCO inputs, all were identified as group 2 (resistance group). A minority of remotor motor neurons were hyperpolarized by octopamine. All of these were identified as group 1 (assistance group), with strong TCMRO input. 9. The majority of promotor motor neurons were depolarized by octopamine. This depolarization was nevertheless inhibitory since it reversed slightly positive to rest and was associated with a substantial fall in inp


2015 ◽  
Vol 114 (2) ◽  
pp. 1090-1101 ◽  
Author(s):  
Philipp Rosenbaum ◽  
Josef Schmitz ◽  
Joachim Schmidt ◽  
Ansgar Büschges

Animals modify their behavior constantly to perform adequately in their environment. In terrestrial locomotion many forms of adaptation exist. Two tasks are changes of walking direction and walking speed. We investigated these two changes in motor output in the stick insect Cuniculina impigra to see how they are brought about at the level of leg motor neurons. We used a semi-intact preparation in which we can record intracellularly from leg motor neurons during walking. In this single-leg preparation the middle leg of the animal steps in a vertical plane on a treadwheel. Stimulation of either abdomen or head reliably elicits fictive forward or backward motor activity, respectively, in the fixed and otherwise deafferented thorax-coxa joint. With a change of walking direction only thorax-coxa-joint motor neurons protractor and retractor changed their activity. The protractor switched from swing activity during forward to stance activity during backward walking, and the retractor from stance to swing. This phase switch was due to corresponding change of phasic synaptic inputs from inhibitory to excitatory and vice versa at specific phases of the step cycle. In addition to phasic synaptic input a tonic depolarization of the motor neurons was present. Analysis of changes in stepping velocity during stance showed only a significant correlation to flexor motor neuron activity, but not to that of retractor and depressor motor neurons during forward walking. These results show that different tasks in the stick insect walking system are generated by altering synaptic inputs to specific leg joint motor neurons only.


2009 ◽  
Vol 102 (2) ◽  
pp. 1180-1192 ◽  
Author(s):  
Matthias Gruhn ◽  
Géraldine von Uckermann ◽  
Sandra Westmark ◽  
Anne Wosnitza ◽  
Ansgar Büschges ◽  
...  

We performed electrophysiological and behavioral experiments in single-leg preparations and intact animals of the stick insect Carausius morosus to understand mechanisms underlying the control of walking speed. At the level of the single leg, we found no significant correlation between stepping velocity and spike frequency of motor neurons (MNs) other than the previously shown modification in flexor (stance) MN activity. However, pauses between stance and swing motoneuron activity at the transition from stance to swing phase and stepping velocity are correlated. Pauses become shorter with increasing speed and completely disappear during fast stepping sequences. By means of extra- and intracellular recordings in single-leg stick insect preparations we found no systematic relationship between the velocity of a stepping front leg and the motoneuronal activity in the ipsi- or contralateral mesothoracic protractor and retractor, as well as flexor and extensor MNs. The observations on the lack of coordination of stepping velocity between legs in single-leg preparations were confirmed in behavioral experiments with intact stick insects tethered above a slippery surface, thereby effectively removing mechanical coupling through the ground. In this situation, there were again no systematic correlations between the stepping velocities of different legs, despite the finding that an increase in stepping velocity in a single front leg is correlated with a general increase in nerve activity in all connectives between the subesophageal and all thoracic ganglia. However, when the tethered animal increased walking speed due to a short tactile stimulus, provoking an escape-like response, stepping velocities of ipsilateral legs were found to be correlated for several steps. These results indicate that there is no permanent coordination of stepping velocities between legs, but that such coordination can be activated under certain circumstances.


1998 ◽  
Vol 79 (6) ◽  
pp. 2977-2985 ◽  
Author(s):  
Dennis E. Brunn ◽  
Antje Heuer

Brunn, Dennis E. and Antje Heuer. Cooperative mechanisms between leg joints of Carausius morosus. II. Motor neuron activity and influence of conditional bursting interneuron. J. Neurophysiol. 79: 2977–2985, 1998. The activity of the motor neuron pools of the protractor coxae muscle and of the thoracic part of the depressor trochanteris muscle during forward walking in the stick insect was investigated, and a spiking local interneuron, able to produce “endogenous bursting” and innervating both motor neuron pools, was identified. Extracellular recordings of the motor neurons innervating the protractor and the thoracic depressor of front, middle, and rear legs, respectively, were made with oil-hook electrodes from the peripheral nerves nl2c and nl4a while the animals were walking on a styrofoam treadwheel. The corresponding leg movements were registered and phase histograms were created with the software Spike2. Intracellular recordings were made in the neuropile of the metathoracic ganglion with glass electrodes filled with the dye Lucifer yellow. In all three legs measured (front, middle, and rear), both motor neuron pools increased their activity during the swing movement. The increase in the activity of the protractor motor neurons started at the end of the stance ∼100 ms before reaching the posterior extreme position (PEP), and the activity of the large-sized depressor motor neurons increased as soon as the tarsus was lifted at the PEP. A local spiking interneuron was identified that excited both motor neuron pools. In 4 of 23 recordings the interneuron started to burst in synchrony with protractor and thoracic depressor motor neurons. During bursting a depolarizing stimulus reinforced and a hyperpolarizing stimulus inhibited the activity of both motor neuron pools. Thus we conclude that the thoracic part of the depressor trochanteris muscle might be a component of the neuromuscular system that shapes the swing movement. The two proximal joints, subcoxal and coxa-trochanter, connected mechanically via the thoracic part of the depressor trochanteris muscle, are also connected neurally by segmental and intersegmental spiking interneurons (this paper) and by nonspiking local interneurons (see companion paper).


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Shankar Ramachandran ◽  
Navonil Banerjee ◽  
Raja Bhattacharya ◽  
Michele L Lemons ◽  
Jeremy Florman ◽  
...  

Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here we show that the C. elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.


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