scholarly journals Maintenance of motor pattern phase relationships in the ventilatory system of the crab

1997 ◽  
Vol 200 (6) ◽  
pp. 963-974
Author(s):  
R Dicaprio ◽  
G Jordan ◽  
T Hampton

The central pattern generator responsible for the gill ventilation rhythm in the shore crab Carcinus maenas can produce a functional motor pattern over a large (eightfold) range of cycle frequencies. One way to continue to generate a functional motor pattern over such a large frequency range would be to maintain the relative timing (phase) of the motor pattern as cycle frequency changes. This hypothesis was tested by measuring the phase of eight events in the motor pattern from extracellular recordings at different rhythm frequencies. The motor pattern was found to maintain relatively constant phase relationships among the various motor bursts in this rhythm over a large (sevenfold) range of cycle frequencies, although two phase-maintaining subgroups could be distinguished. Underlying this phase maintenance is a corresponding change in the time delay between events in the motor pattern ranging from 470 to 1800 ms over a sevenfold (300­2100 ms) change in cycle period. Intracellular recordings from ventilatory neurons indicate that there is very little change in the membrane potential oscillation in the motor neurons with changes in cycle frequency. However, recordings from nonspiking interneurons in the ventilatory central pattern generator reveal that the rate of change of the membrane potential oscillation of these neurons varies in proportion to changes in cycle frequency. The strict biomechanical requirements for efficient pumping by the gill bailer, and the fact that work is performed in all phases of the motor pattern, may require that this motor pattern maintain phase at all rhythm frequencies.

2004 ◽  
Vol 92 (3) ◽  
pp. 1904-1917 ◽  
Author(s):  
Paul S. Katz ◽  
Akira Sakurai ◽  
Stefan Clemens ◽  
Deron Davis

Rhythmic motor patterns are thought to arise through the cellular properties and synaptic interactions of neurons in central pattern generator (CPG) circuits. Yet, when examining the CPG underlying the rhythmic escape response of the opisthobranch mollusc, Tritonia diomedea, we found that the cycle period of the fictive swim motor pattern recorded from the isolated nervous system was not altered by changing the resting membrane potential or the level of spiking activity of any of the 3 known CPG cell types: ventral swim interneuron-B (VSI-B), the dorsal swim interneurons (DSIs), and cerebral neuron 2 (C2). Furthermore, tonic firing in one or more DSIs or C2 evoked rhythmic bursting that did not differ from the cycle period of the motor pattern evoked by nerve stimulation, regardless of the firing frequency. In contrast, the CPG produced a large range of cycle periods as a function of temperature. The temperature sensitivity of the fictive motor pattern produced by the isolated nervous system was similar to the temperature sensitivity of the swimming behavior produced by the intact animal. Thus, although the CPG is capable of producing a wide range of cycle periods under the influence of temperature, the membrane potentials and spiking activity of the identified CPG neurons do not determine the periodicity of the motor pattern. This suggests that the timing of activity in this network oscillator may be determined by a mechanism that is independent of the membrane potentials and spike rate of its constituent neurons.


1999 ◽  
Vol 81 (2) ◽  
pp. 950-953 ◽  
Author(s):  
Ralph A. DiCaprio

Gating of afferent input by a central pattern generator. Intracellular recordings from the sole proprioceptor (the oval organ) in the crab ventilatory system show that the nonspiking afferent fibers from this organ receive a cyclic hyperpolarizing inhibition in phase with the ventilatory motor pattern. Although depolarizing and hyperpolarizing current pulses injected into a single afferent will reset the ventilatory motor pattern, the inhibitory input is of sufficient magnitude to block afferent input to the ventilatory central pattern generator (CPG) for ∼50% of the cycle period. It is proposed that this inhibitory input serves to gate sensory input to the ventilatory CPG to provide an unambiguous input to the ventilatory CPG.


2002 ◽  
Vol 87 (3) ◽  
pp. 1572-1585 ◽  
Author(s):  
Mark A. Masino ◽  
Ronald L. Calabrese

Motor pattern generating networks that produce segmentally distributed motor outflow are often portrayed as a series of coupled segmental oscillators that produce a regular progression (constant phase differences) in their rhythmic activity. The leech heartbeat central pattern generator is paced by a core timing network, which consists of two coupled segmental oscillators in segmental ganglia 3 and 4. The segmental oscillators comprise paired mutually inhibitory oscillator interneurons and the processes of intersegmental coordinating interneurons. As a first step in understanding the coordination of segmental motor outflow by this pattern generator, we describe the functional synaptic interactions, and activity and phase relationships of the heart interneurons of the timing network, in isolated nerve cord preparations. In the timing network, most (∼75%) of the coordinating interneuron action potentials were generated at a primary spike initiation site located in ganglion 4 (G4). A secondary spike initiation site in ganglion 3 (G3) became active in the absence of activity at the primary site. Generally, the secondary site was characterized by a reluctance to burst and a lower spike frequency, when compared with the primary site. Oscillator interneurons in G3 inhibited spike activity at both initiation sites, whereas oscillator interneurons in G4 inhibited spike activity only at the primary initiation site. This asymmetry in the control of spike activity in the coordinating interneurons may account for the observation that the phase of the coordinating interneurons is more tightly linked to the G3 than G4 oscillator interneurons. The cycle period of the timing network and the phase difference between the ipsilateral G3 and G4 oscillator interneurons were regular within individual preparations, but varied among preparations. This variation in phase differences observed across preparations implies that modulated intrinsic membrane and synaptic properties, rather than the pattern of synaptic connections, are instrumental in determining phase within the timing network.


2013 ◽  
Vol 109 (10) ◽  
pp. 2451-2465 ◽  
Author(s):  
Alex H. Williams ◽  
Molly A. Kwiatkowski ◽  
Adam L. Mortimer ◽  
Eve Marder ◽  
Mary Lou Zeeman ◽  
...  

The cardiac ganglion (CG) of Homarus americanus is a central pattern generator that consists of two oscillatory groups of neurons: “small cells” (SCs) and “large cells” (LCs). We have shown that SCs and LCs begin their bursts nearly simultaneously but end their bursts at variable phases. This variability contrasts with many other central pattern generator systems in which phase is well maintained. To determine both the consequences of this variability and how CG phasing is controlled, we modeled the CG as a pair of Morris-Lecar oscillators coupled by electrical and excitatory synapses and constructed a database of 15,000 simulated networks using random parameter sets. These simulations, like our experimental results, displayed variable phase relationships, with the bursts beginning together but ending at variable phases. The model suggests that the variable phasing of the pattern has important implications for the functional role of the excitatory synapses. In networks in which the two oscillators had similar duty cycles, the excitatory coupling functioned to increase cycle frequency. In networks with disparate duty cycles, it functioned to decrease network frequency. Overall, we suggest that the phasing of the CG may vary without compromising appropriate motor output and that this variability may critically determine how the network behaves in response to manipulations.


2002 ◽  
Vol 87 (3) ◽  
pp. 1603-1615 ◽  
Author(s):  
Mark A. Masino ◽  
Ronald L. Calabrese

Considerable experimental and theoretical effort has been exerted to understand how constant intersegmental phase relationships are produced between oscillators in segmentally organized pattern generating networks. The phase relationship between the segmental oscillators in the isolated timing network of the leech heartbeat central pattern generator is quite regular within individual preparations. However, it varies considerably among different preparations. Our goal is to determine how the phase relationships in this network are established. Here we assess whether inherent period differences, as suggested by the excitability-gradient hypothesis, play a role in establishing the phase relationships between the two coupled segmental oscillators of the leech heartbeat timing network. To do this we developed methods for reversibly uncoupling the segmental oscillators (sucrose knife) and pharmacological manipulation of the individual oscillators (split bath). Differences in inherent cycle periods between the third and fourth segmental oscillators (G3 and G4) were present in most (20 of 26) preparations. These period differences correlated with the phase differences observed between the segmental oscillators in the recoupled timing network, such that the oscillator with the faster cycle period, regardless of the segment in which it was located, led in phase in proportion to its period difference with the other oscillator. The phase differences between the original (coupled) and recoupled states of individual preparations were similar. Thus application and removal of the sucrose knife did not alter the period difference between the segmental oscillators in the timing network. Pharmacological manipulation of the uncoupled oscillators to alter the period difference between the oscillators led to similar correlated phase differences in the recoupled timing network. Across all experiments the uncoupled segmental oscillator with the faster cycle period established the cycle period of the timing network when recoupled. In conclusion, our findings indicate that an excitability-gradient plays a role in establishing the phase relationship between the segmental oscillators of the leech heartbeat central pattern generator since inherent period differences present between the oscillators are correlated to the phase relationships of the coupled/recoupled timing network.


1986 ◽  
Vol 55 (5) ◽  
pp. 847-865 ◽  
Author(s):  
R. E. Flamm ◽  
R. M. Harris-Warrick

We investigated the effects of dopamine, octopamine, and serotonin on the motor output of the pyloric circuit in the stomatogastric ganglion of the lobster, Panulirus interruptus. Amines were bath applied at concentrations from 10(-8) to 10(-4) M, and the responses of the six classes of pyloric neurons were monitored both intracellularly and extracellularly. Each amine modified the pyloric motor pattern in a specific way. In addition, dopamine and octopamine were each able to produce different motor patterns at different concentrations. Amine effects on pyloric neurons included initiation and enhancement or inhibition of spike activity, changes in the phase relationships of neurons, and changes in the cycle frequency of the pyloric rhythm. These results show that the motor pattern produced by this well-studied central pattern generator circuit is highly plastic and can be modulated by endogenous biogenic amines.


1986 ◽  
Vol 122 (1) ◽  
pp. 303-321
Author(s):  
M. P. Nusbaum

Serotonin-containing cells 21 and 61 strongly excite a swim central pattern generator (CPG) neurone, cell 208, in nearby segmental ganglia in the leech Macrobdella decora. This excitatory effect is apparently independent of activity in the swim-initiating neurone cell 204, which monosynaptically excites cell 208 (Weeks, 1982b). Cell 208 excites cell 21, apparently directly. This is the first identified direct pathway for feedback from the swim central pattern generator to a swim initiator neurone. Focally applied serotonin has no effect on the soma of cell 208, but causes both excitatory and inhibitory responses in cell 208 when applied to different places within the neuropile. Cell 61 polysynaptically excites distant, posterior cells 208. This excitation is mediated at least in part by the activation of nearby cells 208, which polysynaptically excite posterior cells 208. Cell 208 is dye-coupled intraganglionically to a newly identified pair of neurones, designated cells 18. Cell 208 also excites posterior cells 18, apparently directly. This interaction may be the pathway whereby cell 61 polysynaptically excites posterior cells 208. During swimming, cell 18's membrane potential oscillates in phase with cell 208. Intracellular current injection into cell 18 during swimming perturbs the swim motor pattern. Therefore, cell 18 qualifies as a candidate swim CPG neurone.


1985 ◽  
Vol 54 (1) ◽  
pp. 28-39 ◽  
Author(s):  
D. H. Paul ◽  
B. Mulloney

We describe a type of nonspiking premotor local interneuron (interneuron IA) in the abdominal nervous system of Pacifasticus leniusculus. All of its branches are restricted to one side of the midline. These interneurons are identifiable and occur as bilateral pairs, one neuron on each side of abdominal ganglia 3, 4, and 5. The membrane potential of interneuron IA oscillated in phase with the swimmeret rhythm, a motor pattern generated in each of these ganglia, because the neuron received postsynaptic potentials in phase with the rhythm. Sustained hyperpolarization of an individual interneuron IA initiated generation of the swimmeret rhythm in all the ganglia of a quiescent nervous system. Sustained depolarization stopped the swimmeret rhythm in all the active ganglia of a nervous system that was generating the rhythm. Currents injected into one interneuron reset the rhythm. Comparisons of the shapes of the IA interneurons in different ganglia showed that they are similar to each other and distinct from other local interneurons in these ganglia. Interneuron IA has a large integrative segment and relatively few branches that are largely restricted to the lateral neuropil, to which all other kinds of swimmeret neurons also project. We conclude that this interneuron occurs only once in each hemiganglion in abdominal segments 3, 4, and 5, and that it is identifiable. Furthermore, this interneuron is an essential component of the circuit in each hemiganglion that generates the swimmeret rhythm. The interneuron was dye coupled to a particular identifiable motor neuron and not to any other neurons. The motor neuron was not dye-coupled to any other local interneurons. The ability of this motor neuron to reset the rhythm is attributed to its being electrically coupled to interneuron IA in its ganglion.


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