Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta

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.

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.


1993 ◽  
Vol 69 (5) ◽  
pp. 1583-1595 ◽  
Author(s):  
S. Ryckebusch ◽  
G. Laurent

1. When an isolated metathoracic ganglion of the locust was superfused with the muscarinic cholinergic agonist pilocarpine, rhythmic activity was induced in leg motor neurons. The frequency of this induced rhythm increased approximately linearly from 0 to 0.2 Hz with concentrations of pilocarpine from 10(-5) to 10(-4) M. Rhythmic activity evoked by pilocarpine could be completely and reversibly blocked by 3 x 10(-5) M atropine, but was unaffected by 10(-4) M d-tubocurarine. 2. For each hemiganglion, the observed rhythm was characterized by two main phases: a levator phase, during which the anterior coxal rotator, levators of the trochanter, flexors of the tibia, and common inhibitory motor neurons were active; and a depressor phase, during which depressors of the trochanter, extensors of the tibia, and depressors of the tarsus were active. Activity in depressors of the trochanter followed the activity of the levators of the trochanter with a short, constant interburst latency. Activity in the levator of the tarsus spanned both phases. 3. The levator phase was short compared with the period (0.5-2 s, or 10-20% of the period) and did not depend on the period. The interval between the end of a levator burst and the beginning of the following one thus increased with cycle period. The depressor phase was more variable, and was usually shorter than the interval between successive levator bursts. 4. Motor neurons in a same pool often received common discrete synaptic potentials (e.g., levators of trochanter or extensors of tibia), suggesting common drive during the rhythm. Coactive motor neurons on opposite sides (such as left trochanteral depressors and right trochanteral levators), however, did not share obvious common postsynaptic potentials. Depolarization of a pool of motor neurons during its phase of activity was generally accompanied by hyperpolarization of its antagonist(s) on the same side. 5. Rhythmic activity was generally evoked in both hemiganglia of the metathoracic ganglion, but the intrinsic frequencies of the rhythms on the left and right were usually different. The activity of the levators of the trochanter on one side, however, was strongly coupled to that of the depressors of the trochanter on the other side. 6. The locomotory rhythm was weakly coupled to the ventilatory rhythm such that trochanteral levator activity on either side never occurred during the phase of spiracle opener activity corresponding to inspiration. 7. The rhythmic activity observed in vitro bears many similarities to patterns of neural and myographic activity recorded during walking. The similarities and differences are discussed.


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


1995 ◽  
Vol 198 (2) ◽  
pp. 435-456 ◽  
Author(s):  
A Büschges ◽  
J Schmitz ◽  
U Bässler

Bath application of the muscarinic agonist pilocarpine onto the deafferented stick insect thoracic nerve cord induced long-lasting rhythmic activity in leg motoneurones. Rhythmicity was induced at concentrations as low as 1x10(-4) mol l-1 pilocarpine. The most stable rhythms were reliably elicited at concentrations from 2x10(-3) mol l-1 to 5x10(-3) mol l-1. Rhythmicity could be completely abolished by application of atropine. The rhythm in antagonistic motoneurone pools of the three proximal leg joints, the subcoxal, the coxo-trochanteral (CT) and the femoro-tibial (FT), was strictly alternating. In the subcoxal motoneurones, the rhythm was characterised by the retractor burst duration being correlated with cycle period, whereas the protractor burst duration was almost independent of it. The cycle periods of the rhythms in the subcoxal and CT motoneurone pools were in a similar range for a given preparation. In contrast, the rhythm exhibited by motoneurones supplying the FT joint often had about half the duration. The pilocarpine-induced rhythm was generated independently in each hemiganglion. There was no strict intersegmental coupling, although the protractor motoneurone pools of the three thoracic ganglia tended to be active in phase. There was no stereotyped cycle-to-cycle coupling in the activities of the motoneurone pools of the subcoxal joint, the CT joint and the FT joint in an isolated mesothoracic ganglion. However, three distinct 'spontaneous, recurrent patterns' (SRPs) of motoneuronal activity were reliably generated. Within each pattern, there was strong coupling of the activity of the motoneurone pools. The SRPs resembled the motor output during step-phase transitions in walking: for example, the most often generated SRP (SRP1) was exclusively exhibited coincident with a burst of the fast depressor trochanteris motoneurone. During this burst, there was a switch from subcoxal protractor to retractor activity after a constant latency. The activity of the FT joint extensor motoneurones was strongly decreased during SRP1. SRP1 thus qualitatively resembled the motoneuronal activity during the transition from swing to stance of the middle legs in forward walking. Hence, we refer to SRPs as 'fictive step-phase transitions'. In intact, restrained animals, application of pilocarpine also induced alternating activity in antagonistic motoneurone pools supplying the proximal leg joints. However, there were marked differences from the deafferented preparation. For example, SRP1 was not generated in the latter situation. However, if the ipsilateral main leg nerve was cut, SRP1s reliably occurred. Our results on the rhythmicity in leg motoneurone pools of deafferented preparations demonstrate central coupling in the activity of the leg motoneurones that might be incorporated into the generation of locomotion in vivo.


1976 ◽  
Vol 65 (3) ◽  
pp. 643-668
Author(s):  
W. B. Kristan ◽  
R. L. Calabrese

1. Repeating bursts of motor neurone impulses have been recorded from the nerves of completely isolated nerve cords of the medicinal leech. The salient features of this burst rhythm are similar to those obtained in the semi-intact preparation during swimming. Hence the basic swimming rhythm is generated by a central oscillator. 2. Quantitative comparisons between the impulse patterns obtained from the isolated nerve cord and those obtained from a semi-intact preparation show that the variation in both dorsal to ventral motor neurone phasing and burst duration with swim cycle period differ in these two preparations. 3. The increase of intersegmental delay with period, which is a prominent feature of swimming behaviour of the intact animal, is not seen in either the semi-intact or isolated cord preparations. 4. In the semi-intact preparation, stretching the body wall or depolarizing an inhibitory motor neurone changes the burst duration of excitatory motor neurones in the same segment. In the isolated nerve cord, these manipulations also change the period of the swim cycle in the entire cord. 5. These comparisons suggest that sensory input stabilizes the centrally generated swimming rhythm, determines the phasing of the bursts of impulses from dorsal and ventral motor neurones, and matches the intersegmental delay to the cycle period so as to maintain a constant body shape at all rates of swimming.


1998 ◽  
Vol 79 (1) ◽  
pp. 361-370 ◽  
Author(s):  
Sylvie Baudoux ◽  
Carsten Duch ◽  
Oliver T. Morris

Baudoux, Sylvie, Carsten Duch, and Oliver T. Morris. Coupling of efferent neuromodulatory neurons to rhythmical leg motor activity in the locust. J. Neurophysiol. 79: 361–370, 1998. The spike activity of neuromodulatory dorsal unpaired median (DUM) neurons was analyzed during a pilocarpine-induced motor pattern in the locust. Paired intracellular recordings were made from these octopaminergic neurons during rhythmic activity in hindleg motor neurons evoked by applying pilocarpine to an isolated metathoracic ganglion. This motor pattern is characterized by two alternating phases: a levator phase, during which levator, flexor, and common inhibitor motor neurons spike, and a depressor phase, during which depressor and extensor motor neurons spike. Three different subpopulations of efferent DUM neurons could be distinguished during this rhythmical motor pattern according to their characteristic spike output. DUM 1 neurons, which in the intact animal do not innervate muscles involved in leg movements, showed no change apart from a general increase in spike frequency. DUM 3 and DUM 3,4 neurons produced the most variable activity but received frequent and sometimes pronounced hyperpolarizations that were often common to both recorded neurons. DUM 5 and DUM 3,4,5 neurons innervate muscles of the hindleg and showed rhythmical excitation leading to bursts of spikes during rhythmic activity of the motor neurons, which innervate these same muscles. Sometimes the motor output was coordinated across both sides of the ganglion so that there was alternating activity between levators of both sides. In these cases, the spikes of DUM 5 and DUM 3,4,5 neurons and the hyperpolarization of DUM 3 and DUM 3,4 neurons occurred at particular phases in the motor pattern. Our data demonstrate a central coupling of specific types of DUM neurons to a rhythmical motor pattern. Changes in the spike output of these particular efferent DUM neurons parallel changes in the motor output. The spike activity of DUM neurons thus may be controlled by the same circuits that determine the action of the motor neurons. Functional implications for real walking are discussed.


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.


Neuroglia ◽  
2021 ◽  
Vol 2 (1) ◽  
pp. 57-67
Author(s):  
Cecilia Pankau ◽  
Shelby McCubbin ◽  
Robin L. Cooper

Glia, or glial cells, are considered a vital component of the nervous system, serving as an electrical insulator and a protective barrier from the interstitial (extracellular) media. Certain glial cells (i.e., astrocytes, microglia, and oligodendrocytes) within the CNS have been shown to directly affect neural functions, but these properties are challenging to study due to the difficulty involved with selectively-activating specific glia. To overcome this hurdle, we selectively expressed light-sensitive ion channels (i.e., channel rhodopsin, ChR2-XXL) in glia of larvae and adult Drosophila melanogaster. Upon activation of ChR2, both adults and larvae showed a rapid contracture of body wall muscles with the animal remaining in contracture even after the light was turned off. During ChR2-XXL activation, electrophysiological recordings of evoked excitatory junction potentials within body wall muscles of the larvae confirmed a train of motor nerve activity. Additionally, when segmental nerves were transected from the CNS and exposed to light, there were no noted differences in quantal or evoked responses. This suggests that there is not enough expression of ChR2-XXL to influence the segmental axons to detect in our paradigm. Activation of the glia within the CNS is sufficient to excite the motor neurons.


1991 ◽  
Vol 155 (1) ◽  
pp. 21-35 ◽  
Author(s):  
C. M. Sherff ◽  
B. Mulloney

The crustacean red pigment concentrating hormone (RPCH) has been localized in neurons of the crayfish abdominal nerve cord and modulates the crayfish swimmeret rhythm. An antibody to RPCH labels a small set of cell bodies and axons in each abdominal ganglion. Physiological experiments in which RPCH was perfused into the ganglia of isolated nerve cords showed that RPCH modulated the swimmeret rhythm. In nerve cords that were spontaneously producing the swimmeret rhythm, RPCH lengthened both the period and the duration of bursts of action potentials, but did not alter the phase relationships between bursts in different segments. RPCH did not initiate the swimmeret rhythm in preparations that showed intermittent or no bursting activity. We believe that RPCH is released as a neurotransmitter in the lateral neuropil, where it exerts its effects on the local swimmeret circuits.


2003 ◽  
Vol 89 (3) ◽  
pp. 1245-1255 ◽  
Author(s):  
Dirk Bucher ◽  
Turgay Akay ◽  
Ralph A. DiCaprio ◽  
Ansgar Büschges

Interjoint coordination is essential for proper walking behavior in multi-jointed insect legs. We have shown previously that movement signals from the femur-tibia (FT) joint can shape motor activity of the adjacent coxa-trochanter (CT) joint in the stick insect, Carausius morosus. Here, we present data on the role of position signals from the FT-joint on activity generated in motoneurons (MNs) of the CT-joint. We show that the probability of occurrence of stance (with depression in the CT-joint) or swing movements (with levation in the CT-joint) at the start of walking sequences is influenced by the angle of the FT-joint in the resting animal. We tested the influence of FT-joint angle on pharmacologically induced rhythmic activity of CT-joint depressor (DprTr) and levator (LevTr) MNs. The burst duration, mean spike rate within bursts, and duty cycle for each MN pool were found to depend on FT position. For LevTr MNs, these parameters progressively increased as the FT-joint was moved from extension to flexion, and the opposite was true for DprTr MNs. The cycle period of CT-MN rhythmicity also depended on FT position. In addition, we sometimes observed that the motor output shifted completely to one MN pool at extreme positions, suggesting that the central rhythm-generating network for the CT-joint became locked in one phase. These results indicate that position signals from the FT-joint modulate rhythmic activity in CT-joint MNs partly by having access to central rhythm generating networks of the CT-joint.


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