Bursts of Information: Coordinating Interneurons Encode Multiple Parameters of a Periodic Motor Pattern

2006 ◽  
Vol 95 (2) ◽  
pp. 850-861 ◽  
Author(s):  
Brian Mulloney ◽  
Patricia I. Harness ◽  
Wendy M. Hall
Keyword(s):  
Motor Neurons ◽  
Motor Pattern ◽  
Intrinsic Excitability ◽  
Power Stroke ◽  
Start Time ◽  
Time Duration ◽  
Return Stroke ◽  
Multiple Parameters ◽  
Similar Information ◽  
Phase Progression

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.

Passive Properties of Swimmeret Motor Neurons

1997 ◽  
Vol 78 (1) ◽  
pp. 92-102 ◽  
Author(s):  
Carolyn M. Sherff ◽  
Brian Mulloney
Keyword(s):  
Motor Neurons ◽  
Continuous Production ◽  
Motor Pattern ◽  
Input Resistance ◽  
Membrane Potentials ◽  
Power Stroke ◽  
Return Stroke ◽  
Time Constants ◽  
Large Motor ◽  
Passive Electrical Properties

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.

A separate local pattern-generating circuit controls the movements of each swimmeret in crayfish

1993 ◽  
Vol 70 (6) ◽  
pp. 2620-2631 ◽  
Author(s):  
D. Murchison ◽  
A. Chrachri ◽  
B. Mulloney
Keyword(s):  
Membrane Potential ◽  
Motor Neurons ◽  
Motor Pattern ◽  
Oscillatory Activity ◽  
Power Stroke ◽  
Return Stroke ◽  
Potential Oscillations ◽  
Segmental Ganglion ◽  
Left And Right ◽  
Membrane Potential Oscillations

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.

Modulation of the crayfish swimmeret rhythm by octopamine and the neuropeptide proctolin

1987 ◽  
Vol 58 (3) ◽  
pp. 584-597 ◽  
Author(s):  
B. Mulloney ◽  
L. D. Acevedo ◽  
A. G. Bradbury
Keyword(s):  
Spontaneous Activity ◽  
Motor Neurons ◽  
Nerve Cord ◽  
Ventral Nerve Cord ◽  
Motor Pattern ◽  
Threshold Concentration ◽  
Power Stroke ◽  
Motor Patterns ◽  
Dose Dependent ◽  
Characteristic Motor

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.

Motor Pattern Analysis in the Shore Crab (Carcixus Maexas) Walking Freely in Water and on Land

1987 ◽  
Vol 133 (1) ◽  
pp. 395-414 ◽  
Author(s):  
F. CLARAC ◽  
F. LIBERSAT ◽  
H. J. PFLÜGER ◽  
W. RATHMAYER
Keyword(s):  
Activity Patterns ◽  
Motor Pattern ◽  
Carcinus Maenas ◽  
Excitatory Input ◽  
Motor Neurone ◽  
Shore Crab ◽  
Power Stroke ◽  
Return Stroke ◽  
Motor Neurones ◽  
High Level

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.

scholarly journals Five types of nonspiking interneurons in local pattern-generating circuits of the crayfish swimmeret system

2013 ◽  
Vol 110 (2) ◽  
pp. 344-357 ◽  
Author(s):  
Carmen Smarandache-Wellmann ◽  
Cynthia Weller ◽  
Terrence M. Wright ◽  
Brian Mulloney
Keyword(s):  
Motor Neurons ◽  
Single Copy ◽  
Power Stroke ◽  
Return Stroke ◽  
Local Pattern ◽  
Local Circuit ◽  
Physiological Properties ◽  
Functional Classes ◽  
Nonspiking Interneurons ◽  
Confocal Images

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.

Peptidergic modulation of a multioscillator system in the lobster. I. Activation of the cardiac sac motor pattern by the neuropeptides proctolin and red pigment-concentrating hormone

1989 ◽  
Vol 61 (4) ◽  
pp. 833-844 ◽  
Author(s):  
P. S. Dickinson ◽  
E. Marder
Keyword(s):  
Nervous System ◽  
Motor Neurons ◽  
Motor Pattern ◽  
Stomatogastric Ganglion ◽  
Red Pigment ◽  
Stomatogastric Nervous System ◽  
Two Phase ◽  
Motor Patterns ◽  
Neuronal Element

1. The cardiac sac motor pattern consists of slow and irregular impulse bursts in the motor neurons [cardiac sac dilator 1 and 2 (CD1 and CD2)] that innervate the dilator muscles of the cardiac sac region of the crustacean foregut. 2. The effects of the peptides, proctolin and red pigment-concentrating hormone (RPCH), on the cardiac sac motor patterns produced by in vitro preparations of the combined stomatogastric nervous system [the stomatogastric ganglion (STG), the paired commissural ganglia (CGs), and the oesophageal ganglion (OG)] were studied. 3. Bath applications of either RPCH or proctolin activated the cardiac sac motor pattern when this motor pattern was not already active and increased the frequency of the cardiac sac motor pattern in slowly active preparations. 4. The somata of CD1 and CD2 are located in the esophageal and stomatogastric ganglia, respectively. Both neurons project to all four of the ganglia of the stomatogastric nervous system. RPCH elicited cardiac sac motor patterns when applied to any region of the stomatogastric nervous system, suggesting a distributed pattern generating network with multiple sites of modulation. 5. The anterior median (AM) neuron innervates the constrictor muscles of the cardiac sac. The AM usually functions as a part of the gastric mill pattern generator. However, when the cardiac sac is activated by RPCH applied to the stomatogastric ganglion, the AM neuron becomes active in antiphase with the cardiac sac dilator bursts. This converts the cardiac sac motor pattern from a one-phase rhythm to a two-phase rhythm. 6. These data show that a neuropeptide can cause a neuronal element to switch from being solely a component of one neuronal circuit to functioning in a second one as well. This example shows that peptidergic "reconfiguration" of neuronal networks can produce substantial changes in the behavior of associated neurons.

Multiple Presynaptic and Postsynaptic Sites of Inhibitory Modulation by Myomodulin at ARC Neuromuscular Junctions ofAplysia

2003 ◽  
Vol 89 (3) ◽  
pp. 1488-1502 ◽  
Author(s):  
Irina V. Orekhova ◽  
Vera Alexeeva ◽  
Paul J. Church ◽  
Klaudiusz R. Weiss ◽  
Vladimir Brezina
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Neuromuscular Junctions ◽  
Definitive Evidence ◽  
Multiple Parameters ◽  
Intact Muscle ◽  
Single Arc ◽  
Excitatory Junction Potentials ◽  
K Current ◽  
Neuron Terminals

The functional activity of even simple cellular ensembles is often controlled by surprisingly complex networks of neuromodulators. One such network has been extensively studied in the accessory radula closer (ARC) neuromuscular system of Aplysia. The ARC muscle is innervated by two motor neurons, B15 and B16, which release modulatory peptide cotransmitters to shape ACh-mediated contractions of the muscle. Previous analysis has shown that key to the combinatorial ability of B15 and B16 to control multiple parameters of the contraction is an asymmetry in their peptide modulatory actions. B16, but not B15, releases myomodulin, which, among other actions, inhibits the contraction. Work in single ARC muscle fibers has identified a distinctive myomodulin-activated K current as a candidate postsynaptic mechanism of the inhibition. However, definitive evidence for this mechanism has been lacking. Here, working with the single fibers and then motor neuron-elicited excitatory junction potentials (EJPs) and contractions of the intact ARC muscle, we have confirmed two central predictions of the K-current hypothesis: the myomodulin inhibition of contraction is associated with a correspondingly large inhibition of the underlying depolarization, and the inhibition of both contraction and depolarization is blocked by 4-aminopyridine (4-AP), a potent and selective blocker of the myomodulin-activated K current. However, in the intact muscle, the experiments revealed a second, 4-AP-resistant component of myomodulin inhibition of both B15- and B16-elicited EJPs. This component resembles, and mutually occludes with, inhibition of the EJPs by another peptide modulator released from both B15 and B16, buccalin, which acts by a presynaptic mechanism, inhibition of ACh release from the motor neuron terminals. Direct measurements of peptide release showed that myomodulin also inhibits buccalin release from B15 terminals. At the level of contractions, nevertheless, the postsynaptic K-current mechanism is responsible for much of the myomodulin inhibition of peak contraction amplitude. The presynaptic mechanism, which is most evident during the initial build-up of the EJP waveform, underlies instead an increase of contraction latency.

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