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.

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.

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.

Sustained membrane potential change of uropod motor neurons during the fictive abdominal posture movement in crayfish

1986 ◽  
Vol 56 (3) ◽  
pp. 702-717 ◽  
Author(s):  
M. Takahata ◽  
M. Hisada
Keyword(s):  
Membrane Potential ◽  
Motor Neurons ◽  
Membrane Resistance ◽  
Potential Change ◽  
Quiescent State ◽  
Membrane Potential Change ◽  
Synaptic Potentials ◽  
Nonspiking Interneurons ◽  
Body Rolling ◽  
Dendritic Branches

The occurrence of the uropod steering response as one of the equilibrium reflexes to body rolling in crayfish is significantly facilitated if the stimulus is given while the animal is performing the abdominal posture movement. This facilitation of the descending statocyst pathway by the abdominal posture system takes place between the uropod motor neurons and the statocyst interneurons, which directly project from the brain to the terminal abdominal ganglion where the motor neurons originate. To elucidate the synaptic mechanisms underlying the postural facilitation of the steering response, we analyzed in this study the activity of an identified set of uropod motor neurons during the fictive abdominal extension movement in the whole-animal preparation. Intracellular recordings from the dendritic branches of uropod motor neurons revealed that they were continuously excited during the fictive abdominal extension. The large fast motor neurons usually showed a sustained depolarization of the subthreshold magnitude. The small slow ones showed a suprathreshold sustained depolarization with spikes superimposed. Putative inhibitory motor neurons, on the other hand, showed a sustained hyperpolarization with their spontaneous spike discharge suppressed. The discrete synaptic potentials could hardly be distinguished and, instead, small fluctuations of the membrane potential were observed during the sustained depolarization of both the fast and slow motor neurons. Occasionally, large discrete synaptic potentials could be observed to be superimposed on the sustained depolarization. The occurring frequency of these synaptic potentials showed, however, no significant increase associated with the sustained depolarization. It hence seemed unlikely that these potentials were responsible for producing the sustained depolarization. Their amplitude during the sustained depolarization was smaller than that observed during the quiescent state. The sustained membrane potential change during the fictive abdominal movement was also observed in many neurons other than motor neurons, including local nonspiking interneurons and mechanosensory spiking interneurons. Both motor neurons and interneurons showed a decrease in their membrane resistance during the sustained membrane potential change. We concluded that the sustained depolarization of uropod motor neurons during the fictive abdominal extension was produced by the summation of small chemically transmitted postsynaptic potentials.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

scholarly journals Quantitative Analysis of Walking in a Decapod Crustacean, the Rock Lobster Jasus Lalandii: II. Spatial and Temporal Regulation of Stepping in Driven Walking

1983 ◽  
Vol 107 (1) ◽  
pp. 219-243 ◽  
Author(s):  
C. CHASSERAT ◽  
F. CLARAC
Keyword(s):  
Narrow Range ◽  
Decapod Crustacean ◽  
Power Stroke ◽  
Careful Study ◽  
Rock Lobster ◽  
Return Stroke ◽  
Temporal Regulation ◽  
Belt Speed ◽  
Precise Adjustment ◽  
Wide Range

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.

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