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.

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.

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.

Synaptically Evoked Membrane Potential Oscillations Induced by Substance P in Lamprey Motor Neurons

2002 ◽  
Vol 87 (1) ◽  
pp. 113-121 ◽  
Author(s):  
Erik Svensson ◽  
Sten Grillner ◽  
David Parker
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Protein Kinase ◽  
Substance P ◽  
Receptor Antagonist ◽  
Motor Neurons ◽  
Network Activity ◽  
Membrane Properties ◽  
Potential Oscillations ◽  
Membrane Potential Oscillations

Short-lasting application (10 min) of tachykinin neuropeptides evokes long-lasting (>24 h) modulation of N-methyl-d-aspartate (NMDA)-evoked locomotor network activity in the lamprey spinal cord. In this study, the net effects of the tachykinin substance P on the isolated spinal cord have been examined by recording from motor neurons in the absence of NMDA and ongoing network activity. Brief bath application of substance P (30 s to 2 min) induced irregular membrane potential oscillations in motor neurons. These oscillations consisted of depolarizing and hyperpolarizing phases and were associated with phasic ventral-root activity. The oscillations were blocked by the tachykinin antagonist spantide II. They were also blocked by tetrodotoxin (TTX), suggesting that they were not dependent on intrinsic membrane properties of the motor neurons but were synaptically mediated. Substance P could also have a direct effect, however, because a membrane potential depolarization persisted in the presence of TTX. Protein kinase agonists and antagonists were used to investigate the intracellular pathways through which substance P acted. The oscillations were blocked by the selective protein kinase C (PKC) antagonist chelerythrine. However, the TTX-resistant membrane potential depolarization was not significantly affected by blocking PKC. The protein kinase A and G antagonist H8 did not affect either the oscillations or the direct TTX-resistant membrane potential depolarization. The glutamate receptor antagonist kynurenic acid abolished the substance-P-evoked oscillations, suggesting that they were dependent on glutamate release. The oscillations were abolished or reduced by the AMPA/kainate receptor antagonist 6-cyano-7-nitroquinoxalene-2,3-dione but were only reduced by the NMDA receptor antagonist d-AP5. The oscillations were thus mediated by glutamatergic inputs with a greater dependence on non-NMDA receptors. Blocking glycinergic inputs with strychnine resulted in large depolarizing plateaus and bursts of spikes. The glutamatergic and glycinergic inputs underlying the oscillations are apparently evoked through direct and indirect excitatory effects on inhibitory and excitatory premotor interneurons. Substance P thus has a distributed excitatory effect in the spinal cord. While it can activate premotor networks, this activation alone is not able to evoke a coordinated behaviorally relevant motor output.

Modelling the interrelations between calcium oscillations and ER membrane potential oscillations

1997 ◽  
Vol 63 (2-3) ◽  
pp. 221-239 ◽  
Author(s):  
Marko Marhl ◽  
Stefan Schuster ◽  
Milan Brumen ◽  
Reinhart Heinrich
Keyword(s):  
Membrane Potential ◽  
Calcium Oscillations ◽  
Potential Oscillations ◽  
Membrane Potential Oscillations ◽  
Er Membrane

Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons

1993 ◽  
Vol 70 (1) ◽  
pp. 144-157 ◽  
Author(s):  
R. Klink ◽  
A. Alonso
Keyword(s):  
Membrane Potential ◽  
Entorhinal Cortex ◽  
Inward Rectification ◽  
Voltage Level ◽  
Medial Entorhinal Cortex ◽  
Potential Oscillations ◽  
Subthreshold Oscillations ◽  
Outward Rectification ◽  
Ionic Mechanisms ◽  
Membrane Potential Oscillations

1. Layer II of the medial entorhinal cortex is composed of two electrophysiologically and morphologically distinct types of projection neurons: stellate cells (SCs), which are distinguished by rhythmic subthreshold oscillatory activity, and non-SCs. The ionic mechanisms underlying their differential electroresponsiveness, particularly in the subthreshold range of membrane potentials, were investigated in an "in vitro" slice preparation. 2. In both SCs and non-SCs, the apparent membrane input resistance was markedly voltage dependent, respectively decreasing or increasing at hyperpolarized or subthreshold depolarized potential levels. Thus the neurons displayed inward rectification in the hyperpolarizing and depolarizing range. 3. In the depolarizing range, inward rectification was blocked by tetrodotoxin (TTX, 1 microM) in both types of neurons and thus shown to depend on the presence of a persistent low-threshold Na+ conductance (gNap). However, in the presence of TTX, pronounced outward rectification became manifest in the subthreshold depolarizing range of membrane potentials (positive to -60 mV) in the SCs but not in the non-SCs. 4. The rhythmic subthreshold membrane potential oscillations that were present only in the SCs were abolished by TTX and not by Ca2+ conductance block with Cd2+ or Co2+. Subthreshold oscillations thus rely on the activation of voltage-gated Na+, and not Ca2+, conductances. The Ca2+ conductance block also had no effect on the subthreshold outward rectification. 5. Prominent time-dependent inward rectification in the hyperpolarizing range in the SCs persisted after Na(+)- and Ca2+ conductance block. This rectification was not affected by Ba2+ (1 mM), but was blocked by Cs+ (1-4 mM). Therefore, it is most probably generated by a hyperpolarization-activated cationic current (Q-like current). However, the Q-like current appears to play no major role in the generation of subthreshold rhythmic membrane potential oscillations, because these persisted in the presence of Cs+. 6. On the other hand, in the SCs, the fast, sustained, outward rectification that strongly developed (after Na+ conductance block) at the oscillatory voltage level was not affected by Cs+ but was blocked by Ba2+ (1 mM). Barium was also effective in blocking the subthreshold membrane potential oscillations. 7. In the non-SCs, which do not generate subthreshold rhythmic membrane potential oscillations or manifest subthreshold outward rectification in TTX, Ca2+ conductance block abolished spike repolarization and caused the development of long-lasting Na(+)-dependent plateau potentials at a high suprathreshold voltage level. At this level, where prominent delayed rectification is present, the Na+ plateaus sustained rhythmic membrane potential oscillations.(ABSTRACT TRUNCATED AT 400 WORDS)

Intrinsic Theta-Frequency Membrane Potential Oscillations in Hippocampal CA1 Interneurons of Stratum Lacunosum-Moleculare

1999 ◽  
Vol 81 (3) ◽  
pp. 1296-1307 ◽  
Author(s):  
C. Andrew Chapman ◽  
Jean-Claude Lacaille
Keyword(s):  
Membrane Potential ◽  
Hippocampal Slices ◽  
Stratum Radiatum ◽  
Potential Oscillations ◽  
Spike Threshold ◽  
Hippocampal Ca1 ◽  
Theta Frequency ◽  
Stratum Lacunosum Moleculare ◽  
Membrane Potential Oscillations

Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. The ionic conductances underlying membrane potential oscillations of hippocampal CA1 interneurons located near the border between stratum lacunosum-moleculare and stratum radiatum (LM) were investigated using whole cell current-clamp recordings in rat hippocampal slices. At 22°C, when LM cells were depolarized near spike threshold by current injection, 91% of cells displayed 2–5 Hz oscillations in membrane potential, which caused rhythmic firing. At 32°C, mean oscillation frequency increased to 7.1 Hz. Oscillations were voltage dependent and were eliminated by hyperpolarizing cells 6–10 mV below spike threshold. Blockade of ionotropic glutamate and GABA synaptic transmission did not affect oscillations, indicating that they were not synaptically driven. Oscillations were eliminated by tetrodotoxin, suggesting that Na+ currents generate the depolarizing phase of oscillations. Oscillations were not affected by blocking Ca2+ currents with Cd2+ or Ca2+-free ACSF or by blocking the hyperpolarization-activated current ( I h) with Cs+. Both Ba2+ and a low concentration of 4-aminopyridine (4-AP) reduced oscillations but TEA did not. Theta-frequency oscillations were much less common in interneurons located in stratum oriens. Intrinsic membrane potential oscillations in LM cells of the CA1 region thus involve an interplay between inward Na+ currents and outward K+ currents sensitive to Ba2+ and 4-AP. These oscillations may participate in rhythmic inhibition and synchronization of pyramidal neurons during theta activity in vivo.

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