scholarly journals Modulation of Force during Locomotion: Differential Action of Crustacean Cardioactive Peptide on Power-Stroke and Return- Stroke Motor Neurons

1997 ◽  
Vol 17 (18) ◽  
pp. 6872-6883 ◽  
Author(s):  
Brian Mulloney ◽  
Hisaaki Namba ◽  
Hans-Jürgen Agricola ◽  
Wendy M. Hall
1997 ◽  
Vol 78 (1) ◽  
pp. 92-102 ◽  
Author(s):  
Carolyn M. Sherff ◽  
Brian Mulloney

Sherff, Carolyn M. and Brian Mulloney. Passive properties of swimmeret motor neurons. J. Neurophysiol. 78: 92–102, 1997. Four different functional types of motor neurons innervate each swimmeret: return-stroke excitors (RSEs), power-stroke excitors (PSEs), return-stroke inhibitors (RSIs), and power-stroke inhibitors (PSIs). We studied the structures and passive electrical properties of these neurons, and tested the hypothesis that different types of motor neurons would have different passive properties that influenced generation of the swimmeret motor pattern. Cell bodies of neurons innervating one swimmeret were clustered in two anatomic groups in the same ganglion. The shapes of motor neurons in both groups were similar, despite the differences in locations of their cell bodies and in their functions. Diameters of their axons in the swimmeret nerve ranged from <2 to ∼35 μm. Resting membrane potentials, input resistances, and membrane time constants were recorded with microelectrodes in the processes of swimmeret motor neurons in isolated abdominal nerve cord preparations. Membrane potentials had a median of −59 mV, with 25th and 75th percentiles of −66.0 and −53 mV. The median input resistance was 6.4 MΩ, with 25th and 75th percentiles of 3.4 and 13.7 MΩ. Membrane time constants had a median of 9.3 ms, with 25th and 75th percentiles of 5.7 and 15.0 ms. Excitatory and inhibitory motor neurons had similar passive properties. RSE motor neurons were typically more depolarized than the other types, but the passive properties of RSE, PSE, RSI, and PSI neurons were not significantly different. Membrane time constants measured from cell bodies were briefer than those measured from neuropil processes, but membrane potentials and input resistances were not significantly different. The relative sizes of different motor neurons were measured from the sizes of their impulses recorded extracellularly from the swimmeret nerve. Smaller motor neurons had lower membrane potentials and were more likely to be active in the motor pattern than were large motor neurons. Motor neurons of different sizes had similar input resistances and membrane time constants. Motor neurons that were either oscillating or oscillating and firing in phase with the swimmeret motor pattern had lower average membrane potentials and longer time constants than those that were not oscillating. When the state of the swimmeret system changed from quiescence to continuous production of the motor pattern, the resting potentials, input resistances, and membrane time constants of individual swimmeret motor neurons changed only slightly. On average, both input resistance and membrane time constant increased. These similarities are considered in light of the functional task each motor neuron performs, and a hypothesis is developed that links the brief time constants of these neurons and graded synaptic transmission by premotor interneurons to control of the swimmeret muscles and the performance of the swimmeret system.


2006 ◽  
Vol 95 (2) ◽  
pp. 850-861 ◽  
Author(s):  
Brian Mulloney ◽  
Patricia I. Harness ◽  
Wendy M. Hall

The limbs on different segments of the crayfish abdomen that drive forward swimming are directly controlled by modular pattern-generating circuits. These circuits are linked together by axons of identified coordinating interneurons. We described the distributions of these neurons in each abdominal ganglion and monitored their firing during expression of the swimming motor pattern. We analyzed the timing, the numbers of spikes, and the duration of each burst of spikes in these coordinating neurons. To see what information these neurons encoded, we correlated these parameters with the timing, durations, and strengths of bursts of spikes in motor axons from the same modules. During the power-stroke phase of each output cycle, the anterior-projecting neurons fired bursts of spikes that encoded information about the start-time, duration, and strength of each burst of spikes in power-stroke motor neurons from the same module. When the period and intensity of the motor output fluctuated, the bursts of spikes in these neurons tracked these fluctuations accurately. Each additional spike in these neurons signified an increase in the strength of the power-stroke burst. The posterior-projecting neurons that fired during the return-stroke phase encoded similar information about the return-stroke motor neurons. Although homologous neurons from different ganglia were qualitatively similar, neurons from posterior ganglia fired significantly more spikes per burst than those from more anterior ganglia, a segmental gradient that correlates with the normal posterior-to-anterior phase progression of limb movements. We propose that this gradient and a similar gradient in the durations of bursts in power-stroke motor neurons might reflect a hitherto-undetected difference in the excitation or intrinsic excitability of swimmeret modules in different segments.


1993 ◽  
Vol 70 (6) ◽  
pp. 2620-2631 ◽  
Author(s):  
D. Murchison ◽  
A. Chrachri ◽  
B. Mulloney

1. Within an abdominal segment, the motor output from the segmental ganglion to the swimmerets consists of coordinated bursts of impulses in the separate pools of motor neurons innervating the left and right limbs. This coordinated motor pattern features alternating (out-of-phase) bursts of impulses in the power-stroke (PS) and return-stroke (RS) motor axons that innervate each swimmeret. PS bursts on both sides of each segment occur simultaneously (in-phase), and so RS bursts on both sides are also in-phase. 2. With all intersegmental connections interrupted, isolated abdominal ganglia were able to sustain the normal swimmeret motor pattern of alternating PS/RS activity that was bilaterally in-phase. 3. After an isolated ganglion was surgically bisected down the midline, the isolated hemiganglia that resulted could produce stable, coordinated alternation of PS and RS bursts. 4. The neuropeptide proctolin could induce rhythmic oscillations of membrane potential in swimmeret neurons when spiking was blocked by tetrodotoxin (TTX). For neurons within the same hemiganglion, these oscillations retained the same phase relations they displayed in controls, but the oscillations of neurons in different hemiganglia became uncoordinated. 5. Synaptic transmission between swimmeret neurons in the same hemiganglion persisted in the presence of TTX. Swimmeret interneurons that could activate the pattern-generating circuitry under control conditions could induce membrane-potential oscillations in swimmeret neurons of the same hemiganglion when TTX was present. 6. We conclude that a separate hemisegmental pattern-generating circuit controls the rhythmic PS and RS movements of each swimmeret. Each circuit is located in the same hemiganglion as the population of motor neurons that innervates the local swimmeret. Graded transmission is sufficient to coordinate the timing of oscillatory activity within the hemisegmental circuitry. These hemisegmental circuits are coupled by intersegmental and bilateral coordinating pathways that are dependent on sodium action potentials for their operation.


2013 ◽  
Vol 110 (2) ◽  
pp. 344-357 ◽  
Author(s):  
Carmen Smarandache-Wellmann ◽  
Cynthia Weller ◽  
Terrence M. Wright ◽  
Brian Mulloney

We conducted a quantitative analysis of the different nonspiking interneurons in the local pattern-generating circuits of the crayfish swimmeret system. Within each local circuit, these interneurons control the firing of the power-stroke and return-stroke motor neurons that drive swimmeret movements. Fifty-four of these interneurons were identified during physiological experiments with sharp microelectrodes and filled with dextran Texas red, Neurobiotin, or both. Five types of neurons were identified on the basis of combinations of physiological and anatomical characteristics. Anatomical categories were based on 16 anatomical parameters measured from stacks of confocal images obtained from each neuron. The results support the recognition of two functional classes: inhibitors of power stroke (IPS) and inhibitors of return stroke (IRS). The IPS class of interneuron has three morphological types with similar physiological properties. The IRS class has two morphological types with physiological properties and anatomical features different from the IPS neurons but similar within the class. Three of these five types have not been previously identified. Reviewing the evidence for dye coupling within each type, we conclude that each type of IPS neuron and one type of IRS neuron occur as a single copy in each local pattern-generating circuit. The last IRS type includes neurons that might occur as a dye-coupled pair in each local circuit. Recognition of these different interneurons in the swimmeret pattern-generating circuits leads to a refined model of the local pattern-generating circuit that includes synaptic connections that encode and decode information required for intersegmental coordination of swimmeret movements.


1987 ◽  
Vol 58 (3) ◽  
pp. 584-597 ◽  
Author(s):  
B. Mulloney ◽  
L. D. Acevedo ◽  
A. G. Bradbury

1. The swimmeret system can be excited by perfusing the neuropeptide proctolin through the isolated ventral nerve cord of the crayfish. Previously silent preparations begin to generate a characteristic motor pattern, the swimmeret rhythm, in the nerves that innervate the swimmerets. The response to proctolin is dose dependent and reversible. The threshold concentration of proctolin perfused through the ventral artery is approximately 10(-8) M. The EC50 is 1.6 X 10(-6) M. 2. Proctolin-induced motor patterns have periods and phases similar to those of spontaneously generated motor patterns. The durations of the bursts of impulses in power-stroke motor neurons generated in the presence of proctolin are, however, significantly longer than those that occur during spontaneous activity. 3. DL-Octopamine inhibits the swimmeret system, both when the system is spontaneously active and when it has been excited by proctolin. The inhibition by octopamine is dose dependent and reversible. The threshold for inhibition is approximately 10(-6) M, and the EC50 is approximately 5 X 10(-5) M. 4. Octopamine's effect is mimicked by its agonists, synephrine and norepinephrine. Synephrine has a lower threshold concentration than does octopamine, but norepinephrine is much less effective than octopamine. 5. Octopamine's inhibition is partially blocked by an antagonist, phentolamine. 6. Phentolamine also blocks inhibition of the swimmeret system by inhibitory command interneurons. This block is dose dependent and can be partially overcome by stimulating the command interneurons at higher frequencies. 7. Perfusion with 11 other suspected crustacean neurotransmitters and transmitter analogues did not similarly excite or inhibit the swimmeret system, so we suggest that proctolin and octopamine are transmitters used by the neurons that normally control expression of the swimmeret rhythm.


1983 ◽  
Vol 107 (1) ◽  
pp. 219-243 ◽  
Author(s):  
C. CHASSERAT ◽  
F. CLARAC

Spatial and temporal stepping parameters have been studied in a rocklobster walking on a treadmill moving at a wide range of speeds. The stride and the return stroke (RS) duration remain more or less stable and independent of the belt speed. Nevertheless, these ‘invariant’ parameters can act as spatial and temporal buffers resulting in a very precise adjustment of individual steps. A careful study of the power stroke (PS) duration demonstrates that the rock-lobster, although constrained to walk at an imposed belt speed, continues to correct its leg speed over a narrow range when the speed is considerably different from its natural one. Ipsilateral phases are always speed dependent, with an interleg ascending delay that is almost constant. The contralateral phase between legs of the same pair is approximately constant. Some of the parameters described are greatly influenced by gradual or abrupt variations in the belt speed. For a given speed, there is no absolute significance in the step period and ipsilateral phase. At very slow speeds, the interleg relations are significantly changed and have been studied separately. The metachrony observed at other speeds is discussed in relation to data from other arthropods.


1983 ◽  
Vol 107 (1) ◽  
pp. 189-217 ◽  
Author(s):  
F. CLARAC ◽  
C. CHASSERAT

The study compares the relative validity of the data obtained from two experimental situations, i.e. free walking and driven walking, in relation to leg coordination in Jasus lalandii (Milne-Edwards). The relationship between ipsilateral and contralateral legs during the forward as well as the backward walking sequences has been analysed in the two situations. They operate roughly in opposition. Although little difference in the mean phase values has been observed in the two experimental situations, the strength of coupling is greater in the driven walking animals. The power stroke (PS) duration correlates well with the period, but the return stroke (RS) is more variable and varies according to the leg considered. The phase does not appear to be correlated with the step period during free walking, but is correlated in the treadmill situation. Initially, several of the properties of the single motor unit discharges correlated with movement have identical mean values in both free and driven walking. However, several significant differences have been observed in the intra-burst organization. These differences indicate that the constraint of the treadmill decreases the variability of all parameters and produces a stable and more stereotyped walking pattern.


1995 ◽  
Vol 198 (3) ◽  
pp. 683-700 ◽  
Author(s):  
M Jamon ◽  
F Clarac

Freely walking crayfish, Procambarus clarkii, were studied using a video analysis procedure adapted especially for use with crayfish. The animals were placed in a tank and their homing behaviour was filmed as they returned in a straight line to their shelter. Various sequences were studied at the two following levels. First, the trajectory of each pair of legs (from leg 2 to leg 5) during the step cycle (power stroke and return stroke) was studied to measure stride length and to analyse in detail changes in acceleration. Each leg was found to contribute in a specific manner to locomotion. Second, ipsi- and contralateral leg coordination was investigated. Ipsilateral coordination was found to involve a metachronal organization from front to back in all the walking sequences recorded, whereas contralateral coordination involved, in addition to the weak alternate coupling commonly observed in treadmill walking, another coordination pattern where the legs on each side (legs 3 and 4) are in phase. The results obtained in these free-walking sequences are discussed and compared with those obtained previously, in particular in treadmill situations.


1987 ◽  
Vol 133 (1) ◽  
pp. 395-414 ◽  
Author(s):  
F. CLARAC ◽  
F. LIBERSAT ◽  
H. J. PFLÜGER ◽  
W. RATHMAYER

To whom reprint requests should be addressed. Neuromuscular activity underlying lateral walking was studied in the shore crab Carcinus maenas. Electromyograms (EMGs) were recorded from legs on both the trailing and leading sides during free walking on land and under water in a pool (Figs 1, 2, 6, 7). In a trailing leg, the levator, flexor and closer muscles were active during the return stroke (RS) in alternation with the depressor, extensor and opener muscles which were responsible for the power stroke (PS). In a leading leg a different pattern of activity was observed. The flexor and closer muscles were active during the PS, and the extensor and opener muscles during the RS. Trailing steps were shorter and less variable in duration than leading steps (Figs 2, 3 for walking under water, Fig. 6 for walking on land, see also Fig. 7). A comparison of the activity patterns of the single common motor neurone innervating the opener and the stretcher muscle during trailing and leading showed a difference in burst length and instantaneous frequency (Fig. 2C,D). The discharge of this motor neurone usually lasted longer in leading steps. The discharge frequency started at a high level and then decreased during a trailing step, whereas in a leading step it was irregular (Fig. 8). In all walking situations the stretcher and opener muscles, which share a common excitatory motor neurone, received identical excitatory input (Fig. 4). The discharge frequencies of motor neurones innervating the extensor, the stretcher/opener and the closer muscles were investigated (Fig. 5). For motor neurones active during the PS, the frequency was high at the onset of the burst and then declined gradually. With the exception of the closer muscle, the discharge of motor neurones during the RS was more or less constant during the burst. A comparison between walking under water and on land showed that the overall EMG patterns were essentially similar (Fig. 7). However, on land the PS lasted longer and involved the activation of additional motor neurones in muscles which are innervated by several motor neurones, e.g. the extensor (Fig. 6). During walking on land maximal discharge frequencies up to 350 Hz were recorded. Note: Dedicated to Professor Dr Ernst Florey on the occasion of his 60th birthday.


1993 ◽  
Vol 69 (5) ◽  
pp. 1373-1383 ◽  
Author(s):  
A. Chrachri ◽  
D. M. Neil

1. Extracellular and intracellular recordings from an isolated thoraco-abdominal preparation of the crayfish, Pacifastacus leniusculus, demonstrate that the swimmeret and the abdominal positioning systems can at times be spontaneously coordinated with each other. 2. Two forms of coordination were encountered between these two motor systems. First, some flexor and extensor motor neurons can burst in phase with the swimmeret power-stroke motor neurons. Second, when the flexor motor neurons displayed irregular bursting, the swimmeret rhythm was often inhibited. 3. Both of these two forms of coordination between the swimmeret and the abdominal positioning systems can be induced by depolarization of certain abdominal interneurons. 4. Bath application of oxotremorine increases the frequency of the swimmeret rhythm in a dose-dependent manner. The threshold concentration for this effect is 10(-8) M, and it persists for as long as oxotremorine is present in the bathing solution. 5. At a concentration of 10(-5) M, oxotremorine also induces slow rhythmic activity in the abdominal positioning system consisting of opposite firing between the flexor and extensor motor neurons. 6. Bath application of 10(-5) M oxotremorine also induces two types of interaction between these two abdominal motor systems. In cycle-by-cycle coordination the flexor motor neurons and one extensor motor neuron display rhythmic activity in phase with that of power-stroke motor neurons of the swimmeret system. A slow coordination also occurs with an inhibition of the swimmeret rhythm during the extensor bursts and an excitation during the flexor bursts. 7. Injection of similar doses of oxotremorine into the haemolymph of intact crayfish produces rhythmic abdominal movements that are comparable to the fictive pattern induced in the isolated preparation.


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