The central nervous origin of the swimming motor pattern in embryos of Xenopus laevis

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.

1996 ◽  
Vol 76 (5) ◽  
pp. 3178-3195 ◽  
Author(s):  
R. M. Johnston ◽  
R. B. Levine

1. Larval crawling is a bilaterally symmetrical behavior that involves an anterior moving wave of motor activity in the body wall muscles in conjunction with sequential movements of the abdominal prolegs and thoracic legs. The purpose of this study was to determine whether the larval CNS by itself and without phasic sensory feedback was capable of producing patterned activity associated with crawling. To establish the extent of similarity between the output of the isolated nerve cord and crawling, the motor activity produced in isolated larval nerve cords was compared with the motor activity from freely crawling larvae. 2. When exposed to the muscarinic receptor agonist pilocarpine (1.0 mM), isolated larval nerve cords produced long-lasting rhythmic activity in the motor neurons that supply the thoracic leg, abdominal body wall, and abdominal proleg muscles. The rhythmic activity evoked by pilocarpine was abolished reversibly and completely by bath application of the muscarinic-receptor antagonist atropine (0.01 mM) in conjunction with pilocarpine (1.0 mM), suggesting that the response was mediated by muscarinic-like acetylcholine receptors. 3. Similar to crawling in intact animals, the evoked activity in isolated nerve cords involved bilaterally symmetrical motor activity that progressed from the most posterior abdominal segment to the most anterior thoracic segment. The rhythmic activity in thoracic leg, abdominal proleg, and abdominal body wall motor neurons showed intrasegmental and intersegmental cycle-to-cycle coupling. The average cycle period for rhythmic activity in the isolated nerve cord was approximately 2.5 times slower than the cycle period for crawling in intact larvae, but not more variable. 4. Like crawling in intact animals, in isolated nerve cords, bursting activity in the dorsal body wall motor neurons occurred before activity in ventral/lateral body wall motor neurons within an abdominal segment. The evoked bursting activity recorded from the proleg nerve was superimposed on a high level of tonic activity. 5. In isolated nerve cords, bursts of activity in the thoracic leg levator/extensor motor neurons alternated with bursts of activity in the depressor/flexor motor neurons. The burst duration of the levator/extensor activity was brief and remained relatively steady as cycle period increased. The burst duration of the depressor/ flexor activity occupied the majority of an average cycle and increased as cycle period increased. The phase of both levator/extensor motor nerve activity and depressor/flexor motor nerve activity remained relatively stable over the entire range of cycle periods. The timing and patterning of thoracic leg motor neuron activity in isolated nerve cords quantitatively resembled thoracic leg motor activity in freely crawling larvae. 6. The rhythmic motor activity generated by an isolated larval nerve cord resembled a slower version of normal crawling in intact larvae. Because of the many similarities between activity induced in the isolated nerve cord and the muscle activity and movements of thoracic and abdominal segments during crawling, we concluded that central mechanisms can establish the timing and patterning of the crawling motor pattern and that crawling may reflect the output of a central pattern generating network.


1998 ◽  
Vol 79 (5) ◽  
pp. 2316-2328 ◽  
Author(s):  
C. S. Green ◽  
S. R. Soffe

Green, C. S. and S. R. Soffe. Roles of ascending inhibition during two rhythmic motor patterns in Xenopus tadpoles. J. Neurophysiol. 79: 2316–2328, 1998. We have investigated the effects of ascending inhibitory pathways on two centrally generated rhythmic motor patterns in a simple vertebrate model, the young Xenopus tadpole. Tadpoles swim when touched, but when grasped respond with slower, stronger struggling movements during which the longitudinal pattern of motor activity is reversed. Surgical spinal cord transection to remove all ascending connections originating caudal to the transection (in tadpoles immobilized in α-bungarotoxin) did not affect “fictive” swimming generated more rostrally. In contrast, cycle period and burst duration both significantly increased during fictive struggling. Increases were progressively larger with more rostral transection. Blocking caudal activity with the anesthetic MS222 (pharmacological transection) produced equivalent but reversible effects. Reducing crossed-ascending inhibition selectively, either by midsagittal spinal cord division or rostral cord hemisection (1-sided transection) mimicked the effects of transection. Like transection, both operations increased cycle period and burst duration during struggling but did not affect swimming. The changes during struggling were larger with more rostral hemisection. Reducing crossed-ascending inhibition by spinal hemisection also increased the rostrocaudal longitudinal delay during swimming, and the caudorostral delay during struggling. Weakening inhibition globally with low concentrations of the glycine antagonist strychnine (10–100 nM) did not alter swimming cycle period, burst duration, or longitudinal delay. However, strychnine at 10–60 nM decreased cycle period during struggling. It also increased burst duration in some cases, although burst duration increased as a proportion of cycle period in all cases. Strychnine reduced longitudinal delay during struggling, making rostral and caudal activity more synchronous. At 100 nM, struggling was totally disrupted. By combining our results with a detailed knowledge of tadpole spinal cord anatomy, we conclude that inhibition mediated by the crossed-ascending axons of characterized, glycinergic, commissural interneurons has a major influence on the struggling motor pattern compared with swimming. We suggest that this difference is a consequence of the larger, reversed longitudinal delay and the extended burst duration during struggling compared with swimming.


2017 ◽  
Vol 118 (5) ◽  
pp. 2806-2818 ◽  
Author(s):  
Rachel S. White ◽  
Robert M. Spencer ◽  
Michael P. Nusbaum ◽  
Dawn M. Blitz

Sensory feedback influences motor circuits and/or their projection neuron inputs to adjust ongoing motor activity, but its efficacy varies. Currently, less is known about regulation of sensory feedback onto projection neurons that control downstream motor circuits than about sensory regulation of the motor circuit neurons themselves. In this study, we tested whether sensory feedback onto projection neurons is sensitive only to activation of a motor system, or also to the modulatory state underlying that activation, using the crab Cancer borealis stomatogastric nervous system. We examined how proprioceptor neurons (gastropyloric receptors, GPRs) influence the gastric mill (chewing) circuit neurons and the projection neurons (MCN1, CPN2) that drive the gastric mill rhythm. During gastric mill rhythms triggered by the mechanosensory ventral cardiac neurons (VCNs), GPR was shown previously to influence gastric mill circuit neurons, but its excitation of MCN1/CPN2 was absent. In this study, we tested whether GPR effects on MCN1/CPN2 are also absent during gastric mill rhythms triggered by the peptidergic postoesophageal commissure (POC) neurons. The VCN and POC pathways both trigger lasting MCN1/CPN2 activation, but their distinct influence on circuit feedback to these neurons produces different gastric mill motor patterns. We show that GPR excites MCN1 and CPN2 during the POC-gastric mill rhythm, altering their firing rates and activity patterns. This action changes both phases of the POC-gastric mill rhythm, whereas GPR only alters one phase of the VCN-gastric mill rhythm. Thus sensory feedback to projection neurons can be gated as a function of the modulatory state of an active motor system, not simply switched on/off with the onset of motor activity. NEW & NOTEWORTHY Sensory feedback influences motor systems (i.e., motor circuits and their projection neuron inputs). However, whether regulation of sensory feedback to these projection neurons is consistent across different versions of the same motor pattern driven by the same motor system was not known. We found that gating of sensory feedback to projection neurons is determined by the modulatory state of the motor system, and not simply by whether the system is active or inactive.


1990 ◽  
Vol 330 (1258) ◽  
pp. 329-339 ◽  

Rhythmic motoneuronal activity was recorded from segmental motor nerves of moving (spinal swimming) and paralysed (fictive swimming) spinal dogfish ( Scyliorhinus canicula ), and, in the paralysed preparation, microelectrode recordings were made from spinal cord motoneurons. The motoneurons could be divided into two groups, according to their activity patterns. Group I ( n = 31) were inactive during Active swimming and did not respond to gentle tactile stimulation; when recorded from intracellularly they showed stable to weakly oscillating (< 1 mV) membrane potentials. Group II ( n = 15) fired bursts of action potentials in phase with the motor nerve activity, which were superimposed upon larger (up to 17 mV) depolarizations, and responded to gentle tactile stimulation. Two of these cells discharged also in the interburst interval of the nerve activity. Decreases in cycle period of the Active swimming (i.e. increases in locomotor frequency) were instantaneously accompanied by increases in the amplitude of the rectified and integrated motor nerve signal, which represents peak activity of group II motoneurons, and decreases in the duration of the motor burst. Similar instantaneous changes were seen in the firing frequency and burst duration of individual group II motoneurons. The conformity between unit and population behaviour with changing speed of Active swimming, and the close correspondence observed between the form of the excitatory postsynaptic potentials recorded from individual motoneurons and the form of the integrated neurogram, suggest that the group II motoneurons receive a common excitatory drive. Re- and decruitment of motoneurons were virtually absent during these changes of speed. During unstimulated spinal swimming, regular left—right alternating EMG activity is recorded from the red but not from the white part of the myotome. The ratio of group I to group II motoneurons (31:15) recorded in this study agrees with the previously reported proportion of axons in the spinal motor nerve that project to the white and red muscle fibres, respectively. We suggest, therefore, that group II motoneurons innervate the red and superficial muscle fibres and group I the white fibres. The different activity patterns of the two motoneuronal groups in the spinal fish probably reflect the different ways the red and white muscle systems are used during locomotion


2006 ◽  
Vol 95 (5) ◽  
pp. 3154-3163 ◽  
Author(s):  
S. A. Kautz ◽  
C. Patten ◽  
R. R. Neptune

Recent investigation in persons with clinically complete spinal cord injury has revealed that locomotor activity in one limb can activate rhythmic locomotor activity in the opposite limb. Although our previous research has demonstrated profound influences of the nonparetic limb on paretic limb motor activity poststroke, the potency of interlimb pathways for increasing recruitment of the paretic limb motor pattern is unknown. This experiment tested whether there is an increased propensity for rhythmic motor activity in one limb (pedaling limb) to induce rhythmic motor activity in the opposite limb (test limb) in persons poststroke. Forty-nine subjects with chronic poststroke hemiparesis and twenty controls pedaled against a constant mechanical load with their pedaling leg while we recorded EMG and pedal forces from the test leg. For the experimental conditions, subjects were instructed to either pedal with their test leg (bilateral pedaling) or rest their test leg while it was either stationary or moved anti-phased (unilateral pedaling). In persons poststroke, unilateral pedaling activated a complete pattern of rhythmic alternating muscle activity in the nonpedaling, test leg. This effect was most clearly demonstrated in the most severely impaired individuals. In most of the control subjects, unilateral pedaling activated some muscles in the nonpedaling leg weakly, if at all. We propose that, ipsilateral excitatory pathways associated with contralateral pedaling in control subjects are increasingly up-regulated in both legs in persons with hemiparesis as a function of increased hemiparetic severity. This enhancement of interlimb pathways may be of functional importance since contralateral pedaling induced a complete motor pattern of similar amplitude to the bilateral pattern in both the paretic and nonparetic leg of the subjects with severe hemiparesis.


2001 ◽  
Vol 204 (7) ◽  
pp. 1307-1317 ◽  
Author(s):  
D.L. McLean ◽  
J.R. McDearmid ◽  
K.T. Sillar

Nitric oxide (NO) is a ubiquitous neuromodulator with a diverse array of functions in a variety of brain regions, but a role for NO in the generation of locomotor activity has yet to be demonstrated. The possibility that NO is involved in the generation of motor activity in embryos of the frog Rana temporaria was investigated using the NO donors S-nitroso-n-acetylpenicillamine (SNAP; 100--500 micromol l(−1)) and diethylamine nitric oxide complex sodium (DEANO; 25--100 micromol l(−1)). Immobilised Rana temporaria embryos generate a non-rhythmic ‘lashing’ motor pattern either spontaneously or in response to dimming of the experimental bath illumination. Bath-applied NO donors triggered a qualitatively similar motor pattern in which non-rhythmic motor bursts were generated contra- and ipsilaterally down the length of the body. The inactive precursor of SNAP, n-acetyl-penicillamine (NAP), at equivalent concentrations did not trigger motor activity. NO donors failed to initiate swimming and had no measurable effects on the parameters of swimming induced by electrical stimulation. Intracellular recordings with potassium-acetate-filled electrodes revealed that the bursts of ventral root discharge induced by NO donors were accompanied by phasic depolarisations in motor neurons. During the inter-burst intervals, periods of substantial membrane hyperpolarization below the normal resting potential were observed, presumably coincident with contralateral ventral root activity. With KCl-filled electrodes, inhibitory potentials were strongly depolarising, suggesting that inhibition was Cl(−)-dependent. The synaptic drive seen in motor neurons after dimming of the illumination was very similar to that induced by the NO donors. NADPH-diaphorase histochemistry identified putative endogenous sources of NO in the central nervous system and the skin. Three populations of bilaterally symmetrical neurons were identified within the brainstem. Some of these neurons had contralateral projections and many had axonal processes that projected to and entered the marginal zones of the spinal cord, suggesting that they were reticulospinal.


1999 ◽  
Vol 82 (6) ◽  
pp. 3586-3589 ◽  
Author(s):  
Mark D. Gill ◽  
Peter Skorupski

Spontaneous rhythmic motor output of crayfish thoracic ganglia consists of bursts of activity in antagonistic leg motor neurons (MNs), alternating with a rather slow cycle period (typically ≥20 s). The most common pattern (77% of preparations) consists of long coxal promotor bursts, the duration of which was correlated strongly with cycle period, and relatively short remotor bursts independent of cycle period. Octopamine, at a concentration of 2–30 μM reversibly retarded this rhythm, increasing both cycle period and promotor burst duration. Higher concentrations of octopamine inhibited promotor nerve activity and abolished rhythmic bursting. Phentolamine (10–50 μM) had the opposite effect of decreasing cycle period, mainly by decreasing promotor burst duration. Whereas in the presence of octopamine promotor bursts were lengthened and became even more strongly related to cycle period, phentolamine promoted a more symmetrical rhythm with shorter promotor bursts that were less dependent on cycle period. When octopamine was applied in the presence of phentolamine, there was no significant increase in cycle period or burst duration, although high octopamine concentrations (100 μM) were still capable of inhibiting promotor nerve activity. To our knowledge, pharmacological modulation of a spontaneous locomotor rhythm by an amine antagonist (applied by itself) has not been reported previously. The results raise the testable possibility that phentolamine exerts its modulatory effects by acting as an octopamine antagonist in crayfish thoracic ganglia.


1987 ◽  
Vol 133 (1) ◽  
pp. 111-120 ◽  
Author(s):  
F. Delcomyn

1. Rhythmic motor activity may be recorded in the legs of cockroaches during the execution of several different types of behaviour that involve leg movements. It was examined in detail during searching and walking. 2. During walking, motor activity always consisted of a series of bursts separated by silent periods. During searching, it was usually continual, but modulated in frequency. 3. Sometimes, the motor pattern recorded from a searching leg was burst-like rather than modulated. In these cases, it could nevertheless be reliably distinguished from the motor pattern recorded during walking by a simple analysis of the burst pattern. 4. An analysis of the motor pattern recorded during righting indicated that this pattern was more like that for walking than that for searching. Therefore, searching is not simply walking that lacks certain periodic sensory input due to leg contact with the ground. 5. It is concluded that walking and searching can be reliably distinguished from one another on the basis of an analysis of a record of motor activity in a single leg muscle only. An ability to distinguish between similar types of behaviour on the basis of the motor pattern may prove useful in a variety of experiments.


2019 ◽  
Vol 205 (6) ◽  
pp. 881-895 ◽  
Author(s):  
Stefan Schöneich ◽  
Berthold Hedwig

Abstract We investigated the central nervous coordination between singing motor activity and abdominal ventilatory pumping in crickets. Fictive singing, with sensory feedback removed, was elicited by eserine-microinjection into the brain, and the motor activity underlying singing and abdominal ventilation was recorded with extracellular electrodes. During singing, expiratory abdominal muscle activity is tightly phase coupled to the chirping pattern. Occasional temporary desynchronization of the two motor patterns indicate discrete central pattern generator (CPG) networks that can operate independently. Intracellular recordings revealed a sub-threshold depolarization in phase with the ventilatory cycle in a singing-CPG interneuron, and in a ventilation-CPG interneuron an excitatory input in phase with each syllable of the chirps. Inhibitory synaptic inputs coupled to the syllables of the singing motor pattern were present in another ventilatory interneuron, which is not part of the ventilation-CPG. Our recordings suggest that the two centrally generated motor patterns are coordinated by reciprocal feedforward discharges from the singing-CPG to the ventilation-CPG and vice versa. Consequently, expiratory contraction of the abdomen usually occurs in phase with the chirps and ventilation accelerates during singing due to entrainment by the faster chirp cycle.


2011 ◽  
Vol 105 (4) ◽  
pp. 1671-1680 ◽  
Author(s):  
Ulrike B. S. Hedrich ◽  
Florian Diehl ◽  
Wolfgang Stein

Neuronal release of modulatory substances provides motor pattern generating circuits with a high degree of flexibility. In vitro studies have characterized the actions of modulatory projection neurons in great detail in the stomatogastric nervous system, a model system for neuromodulatory influences on central pattern generators. Less is known about the activities and actions of modulatory neurons in fully functional and richly modulated network settings, i.e., in intact animals. It is also unknown whether their activities contribute to the motor patterns in different behavioral conditions. Here, we show for the first time the activity and effects of the well-characterized modulatory projection neuron 1 (MCN1) in vivo and compare them to in vitro conditions. MCN1 was always spontaneously active, typically in a rhythmic fashion with its firing being interrupted by ascending inhibitions from the pyloric motor circuit. Its activity contributed to pyloric motor activity, because 1) the cycle period of the motor pattern correlated with MCN1 firing frequency and 2) stimulating MCN1 shortened the cycle period while 3) lesioning of the MCN1 axon reduced motor activity. In addition, gastric mill motor activity was elicited for the duration of the stimulation. Chemosensory stimulation of the antennae moved MCN1 away from baseline activity by increasing its firing frequency. Following this increase, a gastric mill rhythm was elicited and the pyloric cycle period decreased. Lesioning the MCN1 axon prevented these effects. Thus modulatory projection neurons such as MCN1 can control the motor output in vivo, and they participate in the processing of exteroceptive sensory information in behaviorally relevant conditions.


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