Natural Neural Output That Produces Highly Variable Locomotory Movements

2006 ◽  
Vol 96 (4) ◽  
pp. 2072-2088 ◽  
Author(s):  
Scott L. Hooper ◽  
Christoph Guschlbauer ◽  
Géraldine von Uckermann ◽  
Ansgar Büschges

We recorded fast extensor tibiae motor neuron activity during single-legged treadmill walking in the stick insect, Carausius morosus. We used this activity to stimulate the extensor muscle motor nerve, observed the resulting extensor muscle contractions under isotonic conditions, and quantified these contractions with a variety of measures. Extensor contractions induced in this manner were highly variable, with contraction measures having SDs of 12 to 51%, and ranges of 82 to 275%, when expressed as percentages of the means, an unexpectedly wide range for a locomotory pattern. Searches for correlations among the contraction measures showed that, in general, this high variability is not reduced by contraction measure covariation. Comparing responses (to identical input) across animals showed that extensor muscles from different animals generally significantly differed from one another. However, correlation analyses on these data suggested that these differences do not indicate that multiple extensor muscle subtypes exist. Extensor muscles instead appear to belong to a single class, albeit one with high animal to animal variability. These data thus provide another well-quantified example (along with Aplysia feeding) of a repetitive but highly variable motor pattern (in contrast to the high rhythmicity and stereotypy present in most other well-quantified repetitive motor patterns). We suggest this high variability could be an adaptive combination of locomotion, active sensing, and crypsis arising from the relatively low demand for locomotion in Carausius behavior, the highly fragmented environment the animal inhabits, and its need to avoid predatory attention.

2007 ◽  
Vol 97 (2) ◽  
pp. 1428-1444 ◽  
Author(s):  
Scott L. Hooper ◽  
Christoph Guschlbauer ◽  
Géraldine von Uckermann ◽  
Ansgar Büschges

Graded muscles produce small twitches in response to individual motor neuron spikes. During the early part of their contractions, contraction amplitude in many such muscles depends primarily on the number of spikes the muscle has received, not the frequency or pattern with which they were delivered. Stick insect ( Carausius morosus) extensor muscles are graded and thus would likely show spike-number dependency early in their contractions. Tonic stimulations of the extensor motor nerve showed that the response of the muscles differed from the simplest form of spike-number dependency. However, these differences actually increased the spike-number range over which spike-number dependency was present. When the motor nerve was stimulated with patterns mimicking the motor neuron activity present during walking, amplitude during contraction rises also depended much more on spike number than on spike frequency. A consequence of spike-number dependency is that brief changes in spike frequency do not alter contraction slope and we show here that extensor motor neuron bursts with different spike patterns give rise to contractions with very similar contraction rises. We also examined in detail the early portions of a large number of extensor motor neuron bursts recorded during single-leg walking and show that these portions of the bursts do not appear to have any common spike pattern. Although alternative explanations are possible, the simplest interpretation of these data is that extensor motor neuron firing during leg swing is not tightly controlled.


2002 ◽  
Vol 205 (17) ◽  
pp. 2591-2603 ◽  
Author(s):  
Eric D. Tytell ◽  
George V. Lauder

SUMMARYThe fast-start escape response is the primary reflexive escape mechanism in a wide phylogenetic range of fishes. To add detail to previously reported novel muscle activity patterns during the escape response of the bichir, Polypterus, we analyzed escape kinematics and muscle activity patterns in Polypterus senegalus using high-speed video and electromyography (EMG). Five fish were filmed at 250 Hz while synchronously recording white muscle activity at five sites on both sides of the body simultaneously (10 sites in total). Body wave speed and center of mass velocity, acceleration and curvature were calculated from digitized outlines. Six EMG variables per channel were also measured to characterize the motor pattern. P. senegalus shows a wide range of activity patterns, from very strong responses, in which the head often touched the tail, to very weak responses. This variation in strength is significantly correlated with the stimulus and is mechanically driven by changes in stage 1 muscle activity duration. Besides these changes in duration, the stage 1 muscle activity is unusual because it has strong bilateral activity, although the observed contralateral activity is significantly weaker and shorter in duration than ipsilateral activity. Bilateral activity may stiffen the body, but it does so by a constant amount over the variation we observed; therefore, P. senegalus does not modulate fast-start wave speed by changing body stiffness. Escape responses almost always have stage 2 contralateral muscle activity, often only in the anterior third of the body. The magnitude of the stage 2 activity is the primary predictor of final escape velocity.


2005 ◽  
Vol 93 (3) ◽  
pp. 1255-1265 ◽  
Author(s):  
Björn Ch. Ludwar ◽  
Marie L. Göritz ◽  
Joachim Schmidt

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.


PLoS ONE ◽  
2021 ◽  
Vol 16 (11) ◽  
pp. e0259097
Author(s):  
Damon J. A. Toth ◽  
Alexander B. Beams ◽  
Lindsay T. Keegan ◽  
Yue Zhang ◽  
Tom Greene ◽  
...  

Background Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) poses a high risk of transmission in close-contact indoor settings, which may include households. Prior studies have found a wide range of household secondary attack rates and may contain biases due to simplifying assumptions about transmission variability and test accuracy. Methods We compiled serological SARS-CoV-2 antibody test data and prior SARS-CoV-2 test reporting from members of 9,224 Utah households. We paired these data with a probabilistic model of household importation and transmission. We calculated a maximum likelihood estimate of the importation probability, mean and variability of household transmission probability, and sensitivity and specificity of test data. Given our household transmission estimates, we estimated the threshold of non-household transmission required for epidemic growth in the population. Results We estimated that individuals in our study households had a 0.41% (95% CI 0.32%– 0.51%) chance of acquiring SARS-CoV-2 infection outside their household. Our household secondary attack rate estimate was 36% (27%– 48%), substantially higher than the crude estimate of 16% unadjusted for imperfect serological test specificity and other factors. We found evidence for high variability in individual transmissibility, with higher probability of no transmissions or many transmissions compared to standard models. With household transmission at our estimates, the average number of non-household transmissions per case must be kept below 0.41 (0.33–0.52) to avoid continued growth of the pandemic in Utah. Conclusions Our findings suggest that crude estimates of household secondary attack rate based on serology data without accounting for false positive tests may underestimate the true average transmissibility, even when test specificity is high. Our finding of potential high variability (overdispersion) in transmissibility of infected individuals is consistent with characterizing SARS-CoV-2 transmission being largely driven by superspreading from a minority of infected individuals. Mitigation efforts targeting large households and other locations where many people congregate indoors might curb continued spread of the virus.


1978 ◽  
Vol 73 (1) ◽  
pp. 47-63 ◽  
Author(s):  
B. M. Bush ◽  
J. P. Vedel ◽  
F. Clarac

In the walking legs of decapod crustaceans, intersegmental reflex actions originate from various joint proprioceptors. The activity of the ‘accessory flexor’ (AF) muscle, which with the myochordotonal organ (MCO) constitutes a muscle proprioceptor for the mero-carpopodite (M-C) joint, is modulated by the sensory discharge of a joint receptor (CB chordotonal organ) for the more proximal, coxo-basal (C-B) joint. Selective mechanical stimulation of the CB organ also reflexly modifies the motor activities of the main M-C flexor and extensor muscles (recorded as EMGs). 1. Dynamic CB stretch (as would occur during a dorso-ventral C-B movement - i.e. ‘depression’ of the limb) stimulates motor discharge to the M-C extensor muscle, while dynamic release of CB (as during a ventrodorsal C-B movement - or leg ‘elevation’) excites the accessory flexor as well as the main flexor muscle. 2. Successive M-C muscle responses to repetitive sinusoidal changes of CB length differ quantitatively according to the direction (stretch or release) of the first CB movement, in some cases increasing but more commonly ‘adapting’ with repetition. 3. Reflex discharge frequencies of the extensor, flexor and accessory flexor motoneurones increase with velocity of CB movement. 4. Eye illumination, and spontaneous or other sources of increased central excitability, generally increase the CB reflex drive to the flexor and accessory flexor muscles and, in parallel, decrease the reflex action on the extensor muscle. The results are discussed in terms of the role of proprioceptive reflexes in intersegmental co-ordination of the leg joints. In particular the significance of the reflex regulation of the myochordotonal receptors, and thereby the gain of the M-C resistance reflexes, is considered in the light of the observed ‘co-activation’ of main flexor and receptor muscle motoneurones.


1982 ◽  
Vol 99 (1) ◽  
pp. 185-196 ◽  
Author(s):  
J. A. Kahn ◽  
A. Roberts

Rhythmic motor nerve activity was recorded in stage 37/38 Xenopus embryos paralysed with curare. The activity was similar to the swimming motor pattern in the following ways: cycle period (40–125 ms), alternation of activity on either side of a segment, rostro-caudal phase lag. Episodes of rhythmic motor activity could be evoked by stimuli that evoke swimming and inhibited by stimuli that normally inhibit swimming. On this basis we conclude that the swimming motor pattern is generated by a central nervous mechanism and is not dependent on sensory feedback. In addition to the swimming pattern, another pattern of motor activity (‘synchrony’) was sometimes recorded in curarized embryos. In this, the rhythmic bursts on either side of a segment occurred in synchrony, and the rhythm period (20–50 ms) was half that in swimming. This was probably not an artifact of curarization as there were indications of a similar pattern in uncurarized embryos. Its function remains unclear.


2019 ◽  
Vol 116 (12) ◽  
pp. 5747-5755 ◽  
Author(s):  
Matthew R. Krause ◽  
Pedro G. Vieira ◽  
Bennett A. Csorba ◽  
Praveen K. Pilly ◽  
Christopher C. Pack

Spike timing is thought to play a critical role in neural computation and communication. Methods for adjusting spike timing are therefore of great interest to researchers and clinicians alike. Transcranial electrical stimulation (tES) is a noninvasive technique that uses weak electric fields to manipulate brain activity. Early results have suggested that this technique can improve subjects’ behavioral performance on a wide range of tasks and ameliorate some clinical conditions. Nevertheless, considerable skepticism remains about its efficacy, especially because the electric fields reaching the brain during tES are small, whereas the likelihood of indirect effects is large. Our understanding of its effects in humans is largely based on extrapolations from simple model systems and indirect measures of neural activity. As a result, fundamental questions remain about whether and how tES can influence neuronal activity in the human brain. Here, we demonstrate that tES, as typically applied to humans, affects the firing patterns of individual neurons in alert nonhuman primates, which are the best available animal model for the human brain. Specifically, tES consistently influences the timing, but not the rate, of spiking activity within the targeted brain region. Such effects are frequency- and location-specific and can reach deep brain structures; control experiments show that they cannot be explained by sensory stimulation or other indirect influences. These data thus provide a strong mechanistic rationale for the use of tES in humans and will help guide the development of future tES applications.


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.


2007 ◽  
Vol 98 (3) ◽  
pp. 1718-1732 ◽  
Author(s):  
Scott L. Hooper ◽  
Christoph Guschlbauer ◽  
Géraldine von Uckermann ◽  
Ansgar Büschges

Understanding how nervous systems generate behavior requires understanding how muscles transform neural input into movement. The stick insect extensor tibiae muscle is an excellent system in which to study this issue because extensor motor neuron activity is highly variable during single leg walking and extensor muscles driven with this activity produce highly variable movements. We showed earlier that spike number, not frequency, codes for extensor amplitude during contraction rises, which implies the muscle acts as a slow filter on the time scale of burst interspike intervals (5–10 ms). We examine here muscle response to spiking variation over entire bursts, a time scale of hundreds of milliseconds, and directly measure muscle time constants. Muscle time constants differ during contraction and relaxation, and contraction time constants, although variable, are always extremely slow (200–700 ms). Models using these data show that extremely slow temporal filtering alone can explain much of the observed transform properties. This work also revealed an unexpected (to us) ability of slow filtering to transform steadily declining inputs into constant amplitude outputs. Examination of the effects of time constant variability on model output showed that variation within an SD primarily altered output amplitude, but variation across the entire range also altered contraction shape. These substantial changes suggest that understanding the basis of this variation is central to predicting extensor activity and that the animal could theoretically vary muscle time constant to match extensor response to changing behavioral need.


2015 ◽  
Vol 113 (6) ◽  
pp. 1921-1940 ◽  
Author(s):  
D. Ryczko ◽  
J. Knüsel ◽  
A. Crespi ◽  
S. Lamarque ◽  
A. Mathou ◽  
...  

In tetrapods, limb and axial movements are coordinated during locomotion. It is well established that inter- and intralimb coordination show considerable variations during ongoing locomotion. Much less is known about the flexibility of the axial musculoskeletal system during locomotion and the neural mechanisms involved. Here we examined this issue in the salamander Pleurodeles waltlii, which is capable of locomotion in both aquatic and terrestrial environments. Kinematics of the trunk and electromyograms from the mid-trunk epaxial myotomes were recorded during four locomotor behaviors in freely moving animals. A similar approach was used during rhythmic struggling movements since this would give some insight into the flexibility of the axial motor system. Our results show that each of the forms of locomotion and the struggling behavior is characterized by a distinct combination of mid-trunk motor patterns and cycle durations. Using in vitro electrophysiological recordings in isolated spinal cords, we observed that the spinal networks activated with bath-applied N-methyl-d-aspartate could generate these axial motor patterns. In these isolated spinal cord preparations, the limb motor nerve activities were coordinated with each mid-trunk motor pattern. Furthermore, isolated mid-trunk spinal cords and hemicords could generate the mid-trunk motor patterns. This indicates that each side of the cord comprises a network able to generate coordinated axial motor activity. The roles of descending and sensory inputs in the behavior-related changes in axial motor coordination are discussed.


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