Tight or Loose Coupling Between Components of the Feeding Neuromusculature of Aplysia?

2005 ◽  
Vol 94 (1) ◽  
pp. 531-549 ◽  
Author(s):  
Yuriy Zhurov ◽  
Klaudiusz R. Weiss ◽  
Vladimir Brezina
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Neuromuscular System ◽  
Loose Coupling ◽  
Tight Coupling ◽  
Feeding Behaviors ◽  
Motor Programs ◽  
Firing Patterns ◽  
Functional Behavior ◽  
Tightly Coupled

Like other complex behaviors, the cyclical, rhythmic consummatory feeding behaviors of Aplysia—biting, swallowing, and rejection of unsuitable food—are produced by a complex neuromuscular system: the animal's buccal mass, with numerous pairs of antagonistic muscles, controlled by the firing of numerous motor neurons, all driven by the motor programs of a central pattern generator (CPG) in the buccal ganglia. In such a complex neuromuscular system, it has always been assumed that the activities of the various components must necessarily be tightly coupled and coordinated if successful functional behavior is to be produced. However, we have recently found that the CPG generates extremely variable motor programs from one cycle to the next, and so very variable motor neuron firing patterns and contractions of individual muscles. Here we show that this variability extends even to higher-level parameters of the operation of the neuromuscular system such as the coordination between entire antagonistic subsystems within the buccal neuromusculature. In motor programs elicited by stimulation of the esophageal nerve, we have studied the relationship between the contractions of the accessory radula closer (ARC) muscle, and the firing patterns of its motor neurons B15 and B16, with those of its antagonist, the radula opener (I7) muscle, and its motor neuron B48. There are two separate B15/B16-ARC subsystems, one on each side of the animal, and these are indeed very tightly coupled. Tight coupling can, therefore, be achieved in this neuromuscular system where required. Yet there is essentially no coupling at all between the contractions of the ARC muscles and those of the antagonistic radula opener muscle. We interpret this result in terms of a hypothesis that ascribes a higher-order benefit to such loose coupling in the neuromusculature. The variability, emerging in the successive feeding movements made by the animal, diversifies the range of movements and thereby implements a trial-and-error search through the space of movements that might be successful, an optimal strategy for the animal in an unknown, rapidly changing feeding environment.

Modeling Neuromuscular Modulation in Aplysia. III. Interaction of Central Motor Commands and Peripheral Modulatory State for Optimal Behavior

2005 ◽  
Vol 93 (3) ◽  
pp. 1523-1556 ◽  
Author(s):  
Vladimir Brezina ◽  
Charles C. Horn ◽  
Klaudiusz R. Weiss
Keyword(s):  
Nervous System ◽  
Motor Neuron ◽  
Motor Neurons ◽  
Functional Performance ◽  
Feeding Strategy ◽  
Neuromuscular System ◽  
Robust Performance ◽  
Neuron Firing ◽  
Variable Environment ◽  
Firing Patterns

Recent work in computational neuroethology has emphasized that “the brain has a body”: successful adaptive behavior is not simply commanded by the nervous system, but emerges from interactions of nervous system, body, and environment. Here we continue our study of these issues in the accessory radula closer (ARC) neuromuscular system of Aplysia. The ARC muscle participates in the animal's feeding behaviors, a set of cyclical, rhythmic behaviors driven by a central pattern generator (CPG). Patterned firing of the ARC muscle's two motor neurons, B15 and B16, releases not only ACh to elicit the muscle's contractions but also peptide neuromodulators that then shape the contractions through a complex network of actions on the muscle. These actions are dynamically complex: some are fast, but some are slow, so that they are temporally uncoupled from the motor neuron firing pattern in the current cycle. Under these circumstances, how can the nervous system, through just the narrow channel of the firing patterns of the motor neurons, control the contractions, movements, and behavior in the periphery? In two earlier papers, we developed a realistic mathematical model of the B15/B16-ARC neuromuscular system and its modulation. Here we use this model to study the functional performance of the system in a realistic behavioral task. We run the model with two kinds of inputs: a simple set of regular motor neuron firing patterns that allows us to examine the entire space of patterns, and the real firing patterns of B15 and B16 previously recorded in a 21/2-h-long meal of 749 cycles in an intact feeding animal. These real patterns are extremely irregular. Our main conclusions are the following. 1) The modulation in the periphery is necessary for superior functional performance. 2) The components of the modulatory network interact in nonlinear, context- and task-dependent combinations for best performance overall, although not necessarily in any particular cycle. 3) Both the fast and the slow dynamics of the modulatory state make important contributions. 4) The nervous system controls different components of the periphery to different degrees. To some extent the periphery operates semiautonomously. However, the structure of the peripheral modulatory network ensures robust performance under all circumstances, even with the irregular motor neuron firing patterns and even when the parameters of the functional task are randomly varied from cycle to cycle to simulate a variable feeding environment. In the variable environment, regular firing patterns, which are fine-tuned to one particular task, fail to provide robust performance. We propose that the CPG generates the irregular firing patterns, which nevertheless are guaranteed to give robust performance overall through the actions of the peripheral modulatory network, as part of a trial-and-error feeding strategy in a variable, uncertain environment.

Neuromuscular Modulation in Aplysia. I. Dynamic Model

2003 ◽  
Vol 90 (4) ◽  
pp. 2592-2612 ◽  
Author(s):  
Vladimir Brezina ◽  
Irina V. Orekhova ◽  
Klaudiusz R. Weiss
Keyword(s):  
Mathematical Modeling ◽  
Steady State ◽  
Motor Neuron ◽  
Dynamic Model ◽  
Motor Neurons ◽  
Neuromuscular System ◽  
Feeding Behaviors ◽  
Cellular Effects ◽  
Dynamical Time ◽  
Physiological Systems

Many physiological systems are regulated by complex networks of modulatory actions. Here we use mathematical modeling and complementary experiments to study the dynamic behavior of such a network in the accessory radula closer (ARC) neuromuscular system of Aplysia. The ARC muscle participates in several types of rhythmic consummatory feeding behavior. The muscle's motor neurons release acetylcholine to produce basal contractions, but also modulatory peptide cotransmitters that, through multiple cellular effects, shape the contractions to meet behavioral demands. We construct a dynamic model of the modulatory network and examine its operation as the motor neurons fire in realistic patterns that change gradually over an hour-long meal and abruptly with switches between the different feeding behaviors. The modulatory effects have very disparate dynamical time scales. Some react to the motor neuron firing only over many cycles of the behavior, but one key effect is fast enough to respond to each individual cycle. Switches between the behaviors are therefore followed by rapid relaxations along some modulatory dimensions but not others. The trajectory of the modulatory state is a transient throughout the meal, ranging widely over regions of the modulatory space not accessible in the steady state. There is a pronounced history-dependency: the modulatory state associated with a cycle of a particular behavior depends on when that cycle occurs and what behaviors preceded it. On average, nevertheless, each behavior is associated with a different modulatory state. In the following companion study, we add a model of the neuromuscular transform to reconstruct and evaluate the actual modulated contraction shapes.

Cycle-to-Cycle Variability of Neuromuscular Activity in Aplysia Feeding Behavior

2004 ◽  
Vol 92 (1) ◽  
pp. 157-180 ◽  
Author(s):  
Charles C. Horn ◽  
Yuriy Zhurov ◽  
Irina V. Orekhova ◽  
Alex Proekt ◽  
Irving Kupfermann ◽  
...  
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Motor Program ◽  
Neuromuscular System ◽  
Motor Programs ◽  
Large Variability ◽  
Implanted Electrodes ◽  
Functional Behavior ◽  
High Level ◽  
Stimulation Of

Aplysia consummatory feeding behavior, a rhythmic cycling of biting, swallowing, and rejection movements, is often said to be stereotyped. Yet closer examination shows that cycles of the behavior are very variable. Here we have quantified and analyzed the variability at several complementary levels in the neuromuscular system. In reduced preparations, we recorded the motor programs produced by the central pattern generator, firing of the motor neurons B15 and B16, and contractions of the accessory radula closer (ARC) muscle while repetitive programs were elicited by stimulation of the esophageal nerve. In other similar experiments, we recorded firing of motor neuron B48 and contractions of the radula opener muscle. In intact animals, we implanted electrodes to record nerve or ARC muscle activity while the animals swallowed controlled strips of seaweed or fed freely. In all cases, we found large variability in all parameters examined. Some of this variability reflected systematic, slow, history-dependent changes in the character of the central motor programs. Even when these trends were factored out, however, by focusing only on the differences between successive cycles, considerable variability remained. This variability was apparently random. Nevertheless, it too was the product of central history dependency because regularizing merely the high-level timing of the programs also regularized many of the downstream neuromuscular parameters. Central motor program variability thus appears directly in the behavior. With regard to the production of functional behavior in any one cycle, the large variability may indicate broad tolerances in the operation of the neuromuscular system. Alternatively, some cycles of the behavior may be dysfunctional. Overall, the variability may be part of an optimal strategy of trial, error, and stabilization that the CNS adopts in an uncertain environment.

Activity of multiple identified motor neurons recorded intracellularly during evoked feedinglike motor programs in Aplysia

1994 ◽  
Vol 72 (4) ◽  
pp. 1794-1809 ◽  
Author(s):  
P. J. Church ◽  
P. E. Lloyd
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Muscle Fibers ◽  
Inhibitory Neuron ◽  
Motor Programs ◽  
Firing Patterns ◽  
Complex Interactions ◽  
Intracellular Stimulation ◽  
Evoked Contractions ◽  
Stimulation Of

1. The firing patterns of 22 motor neurons were determined by simultaneously recording intracellularly from up to 7 neurons during evoked feedinglike buccal motor programs (BMPs). Intracellular stimulation of cerebral-buccal interneuron 2 (CBI-2) or tactile stimulation of the odontophore were used to elicit BMPs in a reduced preparation. 2. Evoked BMPs were identified as either ingestive-like (iBMP) or egestive-like (eBMP) on the basis of their similarity to those previously recorded in select neurons in freely behaving animals. Neurons were divided into the p-group, r-group, or c-group, on the basis of the phase relationships of rhythmic membrane depolarizations and hyperpolarizations during evoked BMPs. Depolarization of the p-, r-, and c-group neurons was associated with radular protraction, retraction, and closure, respectively. With one exception, the motor neurons segregated into the same groups during iBMPs and eBMPs. The exception, B7, was categorized as a c-group neuron during iBMPs, but as an r-group neuron during eBMPs. 3. Every motor neuron exhibited cyclic membrane depolarizations and hyperpolarizations, and over one-half of the neurons fired bursts of action potentials, during both iBMPs and eBMPs. The neurons fired in patterns that would be likely to release both their conventional and peptide transmitters. 4. A marked hyperpolarizing step in the p-group neurons coincident with a depolarization in the r-group neurons was observed during both iBMPs and eBMPs, suggesting a degree of shared premotor circuitry for the two BMPs. 5. A shift in the timing of activity in c-group neurons relative to that in p- and r-group neurons during iBMPs and eBMPs was observed and correlates well with the shift in phase of radular closure relative to protraction and retraction, which is useful in distinguishing ingestion from egestion in the behaving animal. 6. The firing patterns recorded in neurons that innervate overlapping populations of muscle fibers suggested that there would be complex interactions of multiple transmitters. This is particularly intriguing in the case of I3a muscle fibers, which are innervated by two excitatory and one inhibitory neuron. The firing patterns recorded in these neurons suggest that the inhibitory motor neuron may serve to not only block inappropriate contractions, but also to specifically shape evoked contractions during feeding.

scholarly journals Tightly Coupled GNSS/INS Integration with Robust Sequential Kalman Filter for Accurate Vehicular Navigation

Sensors ◽  
2020 ◽  
Vol 20 (2) ◽  
pp. 561 ◽  
Author(s):  
Yi Dong ◽  
Dingjie Wang ◽  
Liang Zhang ◽  
Qingsong Li ◽  
Jie Wu
Keyword(s):  
Kalman Filter ◽  
Computational Efficiency ◽  
Estimation Method ◽  
Accurate Solution ◽  
Global Navigation Satellite Systems ◽  
Loose Coupling ◽  
Tight Coupling ◽  
Integration Model ◽  
Performance Improvements ◽  
Tightly Coupled

With the development of multi-constellation multi-frequency Global Navigation Satellite Systems (GNSS), more and more observations are available for tightly coupled GNSS/Inertial Navigation System (INS) integration. Concerning the accuracy, robustness, and computational burden issues in the integration, we proposed a robust and computationally efficient implementation. The new tight integration model uses pseudorange, Doppler and carrier phase simultaneously, to achieve the maximum possible navigation accuracy for a single receiver. The resultant high-dimensional observation vector is then processed by a sequential Kalman Filter (KF) to improve the computational efficiency in the measurement update step. Based on the innovation of the sequential KF, a robust estimation method with Gaussian test is further devised to detect and adapt the faults in individual GNSS channels. Two field vehicular tests are conducted to evaluate the performance improvements of the proposed method, compared with loose coupling and conventional tight coupling. Test results in favorable environments indicate that the proposed method can significantly improve the velocity and attitude accuracy by 69.42% and 47.16% over loose coupling and by 64.75% and 30.88% over conventional tight coupling, respectively. Moreover, the computational efficiency is also improved by about 53.09% for the proposed method, compared with batch KF processing. In GNSS challenging environments, the proposed method also shows superiority in terms of velocity and attitude accuracy, and better bridging capability during the GNSS partial or complete outages. These results demonstrate that the proposed method is able to provide a more robust and accurate solution in real-time vehicular navigation.

scholarly journals Transsynaptic interactions between IgSF proteins DIP-α and Dpr10 are required for motor neuron targeting specificity

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
James Ashley ◽  
Violet Sorrentino ◽  
Meike Lobb-Rabe ◽  
Sonal Nagarkar-Jaiswal ◽  
Liming Tan ◽  
...  
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Surface Proteins ◽  
Partner Choice ◽  
Neuromuscular System ◽  
Synaptic Specificity ◽  
Binding Partner ◽  
Spatial Expression Pattern ◽  
Muscle Innervation ◽  
Temporal And Spatial

The Drosophila larval neuromuscular system provides an ideal context in which to study synaptic partner choice, because it contains a small number of pre- and postsynaptic cells connected in an invariant pattern. The discovery of interactions between two subfamilies of IgSF cell surface proteins, the Dprs and the DIPs, provided new candidates for cellular labels controlling synaptic specificity. Here we show that DIP-α is expressed by two identified motor neurons, while its binding partner Dpr10 is expressed by postsynaptic muscle targets. Removal of either DIP-α or Dpr10 results in loss of specific axonal branches and NMJs formed by one motor neuron, MNISN-1s, while other branches of the MNISN-1s axon develop normally. The temporal and spatial expression pattern of dpr10 correlates with muscle innervation by MNISN-1s during embryonic development. We propose a model whereby DIP-α and Dpr10 on opposing synaptic partners interact with each other to generate proper motor neuron connectivity.

scholarly journals Transsynaptic interactions between IgSF proteins DIP-α and Dpr10 are required for motor neuron targeting specificity in Drosophila

2018 ◽  
Author(s):  
James Ashley ◽  
Violet Sorrentino ◽  
Sonal Nagarkar-Jaiswal ◽  
Liming Tan ◽  
Shuwa Xu ◽  
...  
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Surface Proteins ◽  
Partner Choice ◽  
Neuromuscular System ◽  
Synaptic Specificity ◽  
Binding Partner ◽  
Spatial Expression Pattern ◽  
Muscle Innervation ◽  
Temporal And Spatial

ABSTRACTThe Drosophila larval neuromuscular system provides an ideal context in which to study synaptic partner choice, because it contains a small number of pre- and postsynaptic cells connected in an invariant pattern. The discovery of interactions between two subfamilies of IgSF cell surface proteins, the Dprs and the DIPs, provided new candidates for cellular labels controlling synaptic specificity. Here we show that DIP-α is expressed by two identified motor neurons, while its binding partner Dpr10 is expressed by postsynaptic muscle targets. Removal of either DIP-α or Dpr10 results in loss of specific axonal branches and NMJs formed by one motor neuron, MNISN-1s, while other branches of the MNISN-1s axon develop normally. The temporal and spatial expression pattern of dpr10 correlates with muscle innervation by MNISN-1s during embryonic development. We propose a model whereby DIP-α and Dpr10 on opposing synaptic partners interact with each other to generate proper motor neuron connectivity.

Rapid Dopaminergic Signaling by Interneurons That Contain Markers for Catecholamines and GABA in the Feeding Circuitry of Aplysia

2005 ◽  
Vol 93 (4) ◽  
pp. 2142-2156 ◽  
Author(s):  
Manuel Díaz-Ríos ◽  
Mark W. Miller
Keyword(s):  
Motor Neurons ◽  
Receptor Agonist ◽  
Input Resistance ◽  
Pattern Generator ◽  
Feeding Behaviors ◽  
Motor Programs ◽  
Pharmacological Tests ◽  
Specific Manner ◽  
Rapid Signaling ◽  
Functional Output

Consummatory feeding behaviors in Aplysia californica are controlled by a polymorphic central pattern generator (CPG) circuit. Previous investigations have demonstrated colocalization of markers for GABA and catecholamines within two interneurons, B20 and B65, that participate in configuring the functional output of this CPG. This study examined the contributions of GABA and dopamine (DA) to rapid synaptic signaling from B20 and B65 to follower cells that implement their specification of motor programs. Pharmacological tests did not substantiate the participation of GABA in the mediation of the excitatory postsynaptic potentials (EPSPs) from either B20 or B65. However, GABA and the GABAB receptor agonist baclofen were found to modify these signals in a target-specific manner. Several observations indicated that DA acts as the neurotransmitter mediating fast EPSPs from B20 to two radula closer motor neurons B8 and B16. In both motor neurons, application of DA produced depolarizing responses associated with decreased input resistance and increased excitation. B20-evoked EPSPs in both follower cells were occluded by exogenous dopamine and blocked by the DA antagonist sulpiride. While dopamine occlusion and sulpiride block of convergent signaling to B8 from B65 resembled that of B20, both of these actions were less potent on the rapid signaling from B65 to the multifunctional and widely acting interneuron B4/5. These findings indicate that dopamine mediates divergent (B20 to B16 and B8) and convergent (B20 and B65 to B8) rapid EPSPs from two influential CPG interneurons in which it is colocalized with GABA-like immunoreactivity.

The Neuromuscular Transform Constrains the Production of Functional Rhythmic Behaviors

2000 ◽  
Vol 83 (1) ◽  
pp. 232-259 ◽  
Author(s):  
Vladimir Brezina ◽  
Klaudiusz R. Weiss
Keyword(s):  
Nervous System ◽  
Motor Neuron ◽  
Preceding Paper ◽  
Limited Range ◽  
Functional Requirements ◽  
Cycle Frequency ◽  
Neuron Firing ◽  
Firing Patterns ◽  
Functional Behavior ◽  
Rhythmic Behaviors

We continue our study of the properties and the functional role of the neuromuscular transform (NMT). The NMT is an input-output relation that formalizes the processes by which patterns of motor neuron firing are transformed to muscle contractions. Because the NMT acts as a dynamic, nonlinear, and modifiable filter, the transformation is complex. In the preceding paper we developed a framework for analysis of the NMT and identified with it principles by which the NMT transforms different firing patterns to contractions. The ultimate question is functional, however. In sending different firing patterns through the NMT, the nervous system is seeking to command different functional behaviors, with specific contraction requirements. To what extent do the contractions that emerge from the NMT actually satisfy those requirements? In this paper we extend our analysis to address this issue. We define representative behavioral tasks and corresponding measures of performance, for a single neuromuscular unit, for two antagonistic units, and, in a real illustration, for the accessory radula closer (ARC)–opener neuromuscular system of Aplysia. We focus on cyclical, rhythmic behaviors which reveal the underlying principles particularly clearly. We find that, although every pattern of motor neuron firing produces some state of muscle contraction, only a few patterns produce functional behavior, and even fewer produce efficient functional behavior. The functional requirements thus dictate certain patterns to the nervous system. But many desirable functional behaviors are not possible with any pattern. We examine, in particular, how rhythmic behaviors degrade and disintegrate as the nervous system attempts to speed up their cycle frequency. This happens because, with fixed properties, the NMT produces only a limited range of contraction shapes that are kinetically well matched to the firing pattern only on certain time scales. Thus the properties of the NMT constrain and restrict the production of functional behaviors. In the following paper, we see how the constraint may be alleviated and the range of functional behaviors expanded by appropriately tuning the properties of the NMT through neuromuscular plasticity and modulation.

Sonometric Measurements of Motor-Neuron-Evoked Movements of an Internal Feeding Structure (the Radula) in Aplysia

2001 ◽  
Vol 86 (2) ◽  
pp. 1057-1061 ◽  
Author(s):  
Irina V. Orekhova ◽  
Jian Jing ◽  
Vladimir Brezina ◽  
Ralph A. DiCaprio ◽  
Klaudiusz R. Weiss ◽  
...  
Keyword(s):  
Motor Neuron ◽  
Motor Neurons ◽  
Neural Control ◽  
Feeding System ◽  
Motor Programs ◽  
Rhythmic Motor ◽  
Feeding Structure ◽  
Intracellular Stimulation ◽  
Functional Movements ◽  
Stimulation Of

In many systems used to study rhythmic motor programs, the structures that generate behavior are at least partially internal. In these systems, it is often difficult to directly monitor neurally evoked movements. As a consequence, although motor programs are relatively well characterized, it is generally less clear how neural activity is translated into functional movements. This is the case for the feeding system of the mollusk Aplysia. Here we used sonomicrometry to monitor neurally evoked movements of the food-grasping organ in Aplysia, the radula. Movements were evoked by intracellular stimulation of motor neurons that innervate radula muscles that have been extensively studied in reduced preparations. Nevertheless our results indicate that the movements and neural control of the radula are more complex than has been assumed. We demonstrate that motor neurons previously characterized as radula openers (B48) and closers (B8, B15, B16) additionally produce other movements. Moreover, we show that the size of the movement evoked by a motor neuron can depend on the preexisting state of the radula. Specifically, the motor neurons B15 and B16 produce large closing movements when the radula is partially open but produce relatively weak closing movements in a preparation at rest. Thus the efficacy of B15 and B16 as radula closers is context dependent.

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