Pattern Generator For Swimming Research Articles

Design, swimming motion planning and implementation of a legged underwater robot (CALEB10: D.BeeBot) by biomimetic approach

In this paper, we propose swimming pattern generator (SPG) which is mimicking locomotion of diving beetles with a view point of bimomimetics for legged underwater robots. Firstly, the locomotion of the diving beetle has been observed and classified through experiments with a motion capture system consist of a high-speed camera and imaging processing software Image J. Subsequently, we analyzed coordinated patterns of rhythmic movements of the diving beetle's leg and formulated equations by employing Fourier least mean square fitting method corresponding to the obtained raw data from the motion capture system. Based on this, control parameters have been determined by understating their characteristics through the procedure of comparing produced swimming trajectories according to varying their values to observed motions of the diving beetle. For extended research of SPG (ESPG) to reduce the number of the parameters, they are expressed in a parameter space based on correlations of individual parameters and a newly configured parameter space is proposed through underwater experiments. Consequently the number of parameters has been successfully reduced for effective real time application of SPG. Furthermore, a six legged underwater robot has been developed by considering structural advantages that diving beetles have for their effective swimming. Underwater experiments have been conducted to confirm the feasibility of the proposed idea.

Swimming Pattern Generator Based on Diving Beetles for Legged Underwater Robots

Swimming Pattern Generator Based on Diving Beetles for Legged Underwater Robots

The hemisegmental locomotor network revisited

The organization of the minimal neuronal substrate capable of generating locomotor rhythmicity in vertebrates is investigated in several species, with an emphasis on identifying evolutionary-conserved features. In lamprey, an eel-like lower vertebrate that swims by undulatory movements of the body, the network has been identified as a recurrent network of excitatory interneurons localized in each spinal hemisegment. This conclusion rested upon the observation that each side of the spinal cord is able to express rhythmic locomotor-related bursting after being surgically separated along the midline, even in the absence of inhibition. An important caveat, however, is that this rhythmicity must be an intrinsic capability of the hemisegmental networks and not a newly acquired property as a result of a plastic remodeling of the network occurring after the lesion. Here we examine this issue by recording the motor output expressed by the electrically activated hemicord in the first minutes after hemisection. We observed clear rhythmic bursting in the frequency range previously linked to the operation of the central pattern generator for swimming. Moreover, we recorded the output of the unilateral networks in the intact spinal cord (i.e. no midline section performed) by activating them with asymmetrical stimulation. We thus conclude that the lamprey hemicord does possess the intrinsic capability of generating the basic rhythmic drive of locomotion. The wider significance of these data stems from the lamprey being a model of axial locomotion, and from the many lesion studies previously performed in other animals.

Longitudinal neuronal organization and coordination in a simple vertebrate: a continuous, semi-quantitative computer model of the central pattern generator for swimming in young frog tadpoles

When frog tadpoles hatch their swimming requires co-ordinated contractions of trunk muscles, driven by motoneurons and controlled by a Central Pattern Generator (CPG). To study this co-ordination we used a 3.5 mm long population model of the young tadpole CPG with continuous distributions of neurons and axon lengths as estimated anatomically. We found that: (1) alternating swimming-type activity fails to self-sustain unless some excitatory interneurons have ascending axons, (2) a rostro-caudal (R-C) gradient in the distribution of excitatory premotor interneurons with short axons is required to obtain the R-C gradient in excitation and resulting progression of motoneuron firing necessary for forward swimming, (3) R-C delays in motoneuron firing decrease if excitatory motoneuron to premotor interneuron synapses are present, (4) these feedback connections and the electrical synapses between motoneurons synchronise motoneuron discharges locally, (5) the above findings are independent of the detailed membrane properties of neurons.

Central pattern generator for swimming in Melibe

The nudibranch mollusc Melibe leonina swims by bending from side to side. We have identified a network of neurons that appears to constitute the central pattern generator (CPG) for this locomotor behavior, one of only a few such networks to be described in cellular detail. The network consists of two pairs of interneurons, termed 'swim interneuron 1' (sint1) and 'swim interneuron 2' (sint2), arranged around a plane of bilateral symmetry. Interneurons on one side of the brain, which includes the paired cerebral, pleural and pedal ganglia, coordinate bending movements toward the same side and communicate via non-rectifying electrical synapses. Interneurons on opposite sides of the brain coordinate antagonistic movements and communicate over mutually inhibitory synaptic pathways. Several criteria were used to identify members of the swim CPG, the most important being the ability to shift the phase of swimming behavior in a quantitative fashion by briefly altering the firing pattern of an individual neuron. Strong depolarization of any of the interneurons produces an ipsilateral swimming movement during which the several components of the motor act occur in sequence. Strong hyperpolarization causes swimming to stop and leaves the animal contracted to the opposite side for the duration of the hyperpolarization. The four swim interneurons make appropriate synaptic connections with motoneurons, exciting synergists and inhibiting antagonists. Finally, these are the only neurons that were found to have this set of properties in spite of concerted efforts to sample widely in the Melibe CNS. This led us to conclude that these four cells constitute the CPG for swimming. While sint1 and sint2 work together during swimming, they play different roles in the generation of other behaviors. Sint1 is normally silent when the animal is crawling on a surface but it depolarizes and begins to fire in strong bursts once the foot is dislodged and the animal begins to swim. Sint2 also fires in bursts during swimming, but it is not silent in non-swimming animals. Instead activity in sint2 is correlated with turning movements as the animal crawls on a surface. This suggests that the Melibe motor system is organized in a hierarchy and that the alternating movements characteristic of swimming emerge when activity in sint1 and sint2 is bound together.

Travelling wave patterns in a model of the spinal pattern generator using spiking neurons

The aim of this study is to produce travelling waves in a planar net of artificial spiking neurons. Provided that the parameters of the waves--frequency, wavelength and orientation--can be sufficiently controlled, such a network can serve as a model of the spinal pattern generator for swimming and terrestrial quadruped locomotion. A previous implementation using non-spiking, sigmoid neurons lacked the physiological plausibility that can only be attained using more realistic spiking neurons. Simulations were conducted using three types of spiking neuronal models. First, leaky integrate-and-fire neurons were used. Second, we introduced a phenomenological bursting neuron. And third, a canonical model neuron was implemented which could reproduce the full dynamics of the Hodgkin-Huxley neuron. The conditions necessary to produce appropriate travelling waves corresponded largely to the known anatomy and physiology of the spinal cord. Especially important features for the generation of travelling waves were the topology of the local connections--so-called off-centre connectivity--the availability of dynamic synapses and, to some extent, the availability of bursting cell types. The latter were necessary to produce stable waves at the low frequencies observed in quadruped locomotion. In general, the phenomenon of travelling waves was very robust and largely independent of the network parameters and emulated cell types.

The Role of the Escape Swim Motor Network in the Organization of Behavioral Hierarchy and Arousal inPleurobranchaea

The escape swimming pattern generator of the notaspid opisthobranch Pleurobranchaea drives a high threshold, override behavior. The pattern generator is integrated with neural networks of other behaviors so as to coordinate unitary behavioral expression and to promote general behavioral arousal. These functions are separately produced by different swim network elements. One set of swim premotor neurons, the A1/A10 ensemble, A3 and IVS, generate the swim pattern and, through corollary activity, suppress potentially conflicting feeding behavior by exerting broad inhibition at major feeding network interneurons. A second set of swim neurons, the serotonergic As1–4 neurons, provides intrinsic neuromodulatory excitation to the swim pattern generator that sustains the escape swim episode through multiple cycles. The As1–4 also provide neuromodulatory excitation to important modulatory, serotonergic cells in the feeding motor network and locomotor network, and may have a general regulatory role in the distributed serotonergic arousal network of the mollusk. The As1–4 appear to be also necessary to both avoidance and orienting turning, and are therefore likely to be critical, multi-functional components upon which much of the organization of the animal's behavior rests.

The Role of the Escape Swim Motor Network in the Organization of Behavioral Hierarchy and Arousal in Pleurobranchaea1

The escape swimming pattern generator of the notaspid opisthobranch Pleurobranchaea drives a high threshold, override behavior. The pattern generator is integrated with neural networks of other behaviors so as to coordinate unitary behavioral expression and to promote general behavioral arousal. These functions are separately produced by different swim network elements. One set of swim premotor neurons, the A1/A10 ensemble, A3 and IVS, generate the swim pattern and, through corollary activity, suppress potentially conflicting feeding behavior by exerting broad inhibition at major feeding network interneurons. A second set of swim neurons, the serotonergic As1–4 neurons, provides intrinsic neuromodulatory excitation to the swim pattern generator that sustains the escape swim episode through multiple cycles. The As1–4 also provide neuromodulatory excitation to important modulatory, serotonergic cells in the feeding motor network and locomotor network, and may have a general regulatory role in the distributed serotonergic arousal network of the mollusk. The As1–4 appear to be also necessary to both avoidance and orienting turning, and are therefore likely to be critical, multi-functional components upon which much of the organization of the animal's behavior rests.

Evidence that the Central Pattern Generator for Swimming inTritoniaArose from a Non-Rhythmic Neuromodulatory Arousal System: Implications for the Evolution of Specialized Behavior

Evidence that the Central Pattern Generator for Swimming in<i>Tritonia</i>Arose from a Non-Rhythmic Neuromodulatory Arousal System: Implications for the Evolution of Specialized Behavior

Evidence that the Central Pattern Generator for Swimming in Tritonia Arose from a Non-Rhythmic Neuromodulatory Arousal System: Implications for the Evolution of Specialized Behavior1

Comparisons of the nervous systems of closely related invertebrate species show that identified neurons tend to be highly conserved even though the behaviors in which they participate vary. All opisthobranch molluscs examined have a similar set of serotonin-immunoreactive neurons located medially in the cerebral ganglion. In a small number of species, these neurons have been physiologically and morphologically identified. In the nudibranch, Tritonia diomedea, three of the neurons (the dorsal swim interneurons, DSIs) have been shown to be members of the central pattern generator (CPG) underlying dorsal/ventral swimming. The DSIs act as intrinsic neuromodulators, altering cellular and synaptic properties within the swim CPG circuit. Putative homologues of the DSIs have been identified in a number of other opisthobranchs. In the notaspid, Pleurobranchaea californica, the apparent DSI homologues (As1–3) play a similar role in the escape swim and they also have widespread actions on other systems such as feeding and ciliary locomotion. In the gymnosomatid, Clione limacina, the presumed homologous neurons (Cr-SP) are not part of the swimming pattern generator, which is located in the pedal ganglia, but act as extrinsic modulators, responding to noxious stimuli and increasing the frequency of the swim motor program. Putative homologous neurons are also present in non-swimming species such as the anaspid, Aplysia californica, where at least one of the cerebral serotonergic neurons, CC3 (CB-1), evokes neuromodulatory actions in response to noxious stimuli. Thus, the CPG circuit in Tritonia appears to have evolved from the interconnections of neurons that are common to other opisthobranchs where they participate in arousal to noxious stimuli but are not rhythmically active.

Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye.

When the light is dimmed, the pineal eye of hatchling Xenopus laevis tadpoles excites the central pattern generator for swimming, but the behavioural significance of pineal excitation is unclear. We show that tadpoles spend 99 % of their time hanging from the surface meniscus or solid objects using mucus secreted by a cement gland on the head. Attachment inhibits swimming, but unattached tadpoles swim spontaneously. Provided that their pineal eye is intact, they attach closer to the water surface in the dark than in the light and attach preferentially to the underside of floating objects that cast shadows. Dimming causes tadpoles swimming horizontally to turn upwards and is very effective in initiating upward swimming in unattached tadpoles. Similar pineal-dependent responses during swimming are present up to stage 44. Pinealectomy blocks responses to dimming at all stages. Recordings from immobilised tadpoles reveal that light dimming induces faster fictive swimming and that pineal activity is increased for up to 20 min during sustained light dimming. We suggest that the increase in pineal discharge during dimming increases the probability of upward swimming and, in this way, increases the probability of tadpoles attaching to objects higher in the water column that cast shadows.

Analysis of the central pattern generator for swimming in the mollusk Clione.

The pteropod mollusk Clione limacina swims by rhythmic movements of two wings. The central pattern generator (CPG) for swimming, located in the pedal ganglia, is formed by three groups of interneurons. The interneurons of the groups 7 and 8 are of crucial importance for rhythm generation. They are endogenous oscillators capable of generating rhythmic activity with a range of frequencies typical of swimming after extraction from the ganglia. This endogenous rhythmic activity is enhanced by serotonin. The interneurons 7 and 8 produce one prolonged action potential (about 100 ms in duration) per cycle. Prolonged action potentials contribute to determining the duration of the cycle phases. The interneurons of two groups inhibit one another determining their reciprocal activity. The putative transmitters of groups 7 and 8 interneurons are glutamate and acetylcholine, respectively. Transition from one phase to the other is facilitated by the plateau interneurons of group 12 that contribute to termination of one phase and to initiation of the next phase. Maintaining the rhythm generation and transition from one phase to the other is also promoted by postinhibitory rebound. The redundant organization of the swimming generator guarantees the high reliability of its operation. Generation of the swimming output persisted after the inhibitory input from interneurons 8 to 7 had been blocked by atropine. Activity of the swimming generator is controlled by a set of command neurons that activate, inhibit or modulate the operation of the swimming CPG in relation to a behaviorally relevant context.

The Neuronal Basis of the Behavioral Choice between Swimming and Shortening in the Leech: Control Is Not Selectively Exercised at Higher Circuit Levels

Swimming and the whole-body shortening reflex are two incompatible behaviors performed by the medicinal leech Hirudo medicinalis. We set out to examine the neuronal basis of the choice between these behaviors, taking advantage of the fact that the neuronal circuit underlying swimming is relatively well understood. The leech swim circuit is organized hierarchically and contains three interneuronal levels, including two upper levels of "command-like" neurons. We tested the responses of the swim circuit neurons to stimuli that produced shortening, using reduced preparations in which neurophysiological recording could be performed while behaviors were elicited. We found that the majority of the swim circuit neurons, including most of the command-like cells and all of the cells at the highest hierarchical level of the circuit, were excited by stimuli that produced shortening as well as by stimuli that produced swimming. Only a subset of neurons, at levels below the top, were inhibited during shortening; these included one of the command-like cells and an oscillator cell (an interneuron that is part of the central pattern generator for swimming). These results imply that the control of the choice between swimming and shortening is not exercised selectively at the higher levels of the swim circuit.

Neuronal elements that mediate escape swimming and suppress feeding behavior in the predatory sea slug Pleurobranchaea.

1. The white, bilaterally paired A1 interneurons of the cerebropleural ganglion of Pleurobranchaea californica fire rhythmic bursts of action potentials during escape swimming behavior. We studied the role of the A1s in swimming behavior and pattern generation in whole animal and isolated CNS preparations. 2. The escape swim is a cyclic sequence of dorsal and ventral flexions of the body. During the swim, A1 bursts precede and accompany the dorsal flexion phase of the cycle. Hyperpolarization of A1 to prevent spike activity interrupts swimming behavior in the whole animal and fictive swimming in the isolated CNS. Stimulated A1 activity was not observed to cause swimming in whole animals, and was only occasionally sufficient to trigger fictive swimming activity in the isolated CNS. 3. In quiescent whole animal preparations, stimulation of a single A1 normally causes a single dorsal flexion followed by body flexion to the side contralateral to the stimulated cell; characteristically, A1 spike activity stimulates feedback inhibition coinciding with the end of dorsal flexion and the onset of contralateral flexion. 4. A1 spike activity suppresses feeding behavior and causes proboscis retraction in whole animal preparations induced to feed. A1 activity also suppresses fictive feeding driven by stimulation of the critical phasic paracerebral neurons (PCps) of the motor network of feeding in the isolated CNS. Concomitantly, A1 spikes cause potent inhibition of the PCp interneurons. 5. The A1s are specifically excited by noxious mechanical and chemical stimuli, but are not affected by feeding stimuli or the occurrence of feeding behavior. 6. We conclude that the A1 neurons are elements of an escape swimming pattern generator, and that they are probably homologous to the similar C2 neurons of the nudibranch Tritonia diomedea. One of their functions outside of generating the swim pattern may be the suppression of feeding behavior in response to noxious stimulation. These observations provide a neural mechanism for the original observations of the dominance of escape swimming behavior over feeding.

Properties of networks controlling locomotion and significance of voltage dependency of NMDA channels: stimulation study of rhythm generation sustained by positive feedback

1. We have built a realistic 24-neuron model based on data from the spinal pattern generator for swimming in Xenopus embryos with the use of the SWIM programs. The neurons have dendrite, soma, and axon compartments with voltage-gated Na+ and K+ channels. Dendritic synapses were modeled as modulated ionic conductances with currents that have different reversal levels. One of these conductances was voltage dependent to model N-methyl-D-aspartate ("NMDA") synapses in the presence of Mg2+. 2. In this model, rhythm generation is initiated by a brief excitation, depends on rebound from reciprocal inhibition, and is sustained by long-duration "NMDA-dependent" feedback excitation. 3. Without NMDA voltage dependency, rhythmic activity is stable over a wide range of synaptic conductances. Its frequency decreases with more inhibition and increases with more excitation. The introduction of normally distributed variation in soma size or excitatory synaptic conductance extends the lower stable frequency range. Without such variation the frequency of the 24-neuron model is the same as a 4-neuron model provided that the synaptic conductances for each neuron are the same. 4. The effect of introducing NMDA voltage dependency on rebound after negative current injections or synaptic inhibition was investigated in single depolarized model neurons. With NMDA voltage dependency, hyperpolarizations and rebound spike responses were increased. 5. Network activity with NMDA voltage dependency was similar to that without it, but inhibitory postsynaptic potentials (IPSPs) and spikes were larger, and frequencies were lower and more sensitive to changes in excitatory and inhibitory conductance. 6. We conclude that in the model, mutual reexcitation among excitatory spinal interneurons can sustain rhythm generation by positive feedback and that NMDA voltage dependency can enhance postinhibitory rebound, stabilize swimming activity and extend its lower frequency range, and steepen the dependency of frequency on synaptic drive.

Positive feedback as a general mechanism for sustaining rhythmic and non-rhythmic activity

Our aim is to reassess our proposal that various states of motor output may be sustained by positive feedback generated within the premotor neural circuitry. The evidence for this proposal came from the Xenopus embryo which when touched can swim for many seconds even after all movement has been prevented by a neuromuscular blocking agent. Experiments showed that even the spinal cord could sustain its own swimming activity for a few seconds after stimulation. We proposed that this was the result of the glutamatergic excitatory spinal interneurons synapsing with each other. Because this excitation is of long duration compared to the swimming cycle period it can sum from cycle to cycle to sustain swimming by a form of positive feedback. We have tested the plausibility of these ideas by making realistic computer simulations of the spinal networks and have shown that positive feedback can sustain stable swimming activity. Pharmacological evidence recently suggested that acetylcholine contributes to the excitation underlying swimming in spinal embryos so we investigated the central synapses made by motoneurons. Recordings from pairs of synergistic motoneurons then showed: a) cholinergic chemical synapses from more rostral motoneurons activate nicotinic receptors and produce excitation; and b) local intrasegmental electrical synapses also lead to mutual excitation. The presence of central motoneuron synapses suggested that they could contribute to excitation during swimming. We therefore used local drug applications to see if spinal neurons received cholinergic or electrical excitation during fictive swimming. The results show that motoneurons received both types of excitation while interneurons received only cholinergic excitation. This evidence suggests that when motoneurons are active during swimming they contribute positive feedback excitation not only to themselves but also to the premotor interneurons of the spinal rhythm generating network. This excitation would sum with that from ‘glutamatergic’ excitatory interneurons. We conclude that in addition to our original proposal of feedback between excitatory interneurons, there are other forms of positive feedback during swimming in the Xenopus embryo spinal cord. Motoneurons feed excitation back to each other. They may also contribute cholinergic excitation to premotor interneurons which could sum with the excitation from ‘glutamatergic’ interneurons and help to sustain swimming. If they do this, motoneurons may be a component part of the central pattern generator for swimming. Since central motoneuron synapses are a feature of most vertebrat groups, these results suggest a reevaluation of such synapses in these groups also.

Effects of strychnine on fictive swimming in the lamprey: evidence for glycinergic inhibition, discrepancies with model predictions, and novel modulatory rhythms

1. Inhibitory postsynaptic potentials (ipsps) produced by two classes of interneurons, CC (Contralateral and caudal projecting) and lateral interneurons, were tested for strychnine sensitivity using paired intracellular recordings in the lamprey spinal cord. The ipsps were partially blocked by 0.2-0.5 microM strychnine and were completely blocked by 5 microM strychnine. Thus, the ipsps may be glycinergic. 2. These interneurons are key participants in a proposed circuit model for fictive swimming. A connectionist-type computer simulation of the model demonstrated that the cycle period of the network increased with decreasing ipsp strength. 3. Application of strychnine (0.1-0.5 microM) to the spinal cord during fictive swimming induced by an excitatory amino acid increased cycle period, consistent with previous reports, but at odds with stimulation predictions. 4. Strychnine also produced slow rhythmic modulation of fictive swimming (period = 12 s) which maintained left-right alternation and rostral-caudal coordination. Auto- and cross-correlation analyses revealed that the slow modulation was present in a weaker form in most control preparations during fictive swimming. 5. Since the proposed model for the swimming pattern generator in the lamprey spinal cord does not predict the observed speeding with strychnine, nor the slow modulatory rhythm, it appears to be deficient in its present formulation.

Descending serotonergic spinal projections and modulation of locomotor rhythmicity in Rana temporaria embryos.

The neuroanatomy of descending spinal projections from serotonergic raphe interneurons in embryos of the amphibian, Rana temporaria, has been examined around the time of hatching by using immunocytochemical techniques. The results illustrate that at this early stage in development the ventrolateral spinal cord is richly innervated by 5HT immunoreactive (5HTi) raphe spinal axons and associated growth cones. Other regions are devoid of processes. In conjunction, the effects of bath applied 5-hydroxytryptamine (5HT, serotonin) and its metabolic precursor, 5-hydroxytryptophan (5HTP) on locomotor activity, was also investigated by monitoring ventral root activity during fictive swimming in immobilized animals. Fictive swimming activity is similarly modulated by both exogenously applied 5HT and enhanced endogenous release of 5HT (using 5HTP). These agents increase the duration and intensity of ventral root burst, decrease cycle frequency, lengthen rostrocaudal phase delays and reduce swimming episode duration. We conclude that by the time of hatching in Rana temporaria a functional endogenous serotonergic system is established in the spinal cord which modulates the output of the central pattern generator for swimming. We compare and contrast these results with homologous descending pathways in other vertebrates, especially in a related amphibian Xenopus laevis at equivalent stages in development.

The stopping response of Xenopus laevis embryos: pharmacology and intracellular physiology of rhythmic spinal neurones and hindbrain neurones.

1. Xenopus laevis embryos stop swimming in response to pressure on the cement gland. This behaviour and 'fictive' stopping are blocked by bicuculline (10 mumol 1(-1)), tubocurarine (110 mumol 1(-1)) and kynurenic acid (0.5 mmol 1(-1)). 2. Intracellular recordings from spinal neurones active during swimming have shown that pressure on the cement gland evokes compound, chloride-dependent inhibitory postsynaptic potentials (IPSPs). These are blocked by bicuculline, tubocurarine and kynurenic acid, but are unaffected by strychnine (2 mumol 1(-1)). 3. When the cement gland is pressed, trigeminal ganglion activity precedes both the IPSPs and the termination of 'fictive' swimming activity recorded in rhythmic spinal neurones. The trigeminal discharge is unaffected by the antagonists bicuculline, tubocurarine, kynurenic acid and strychnine. 4. Intracellular recordings from the hindbrain have revealed neurones that are normally silent, but rhythmically inhibited during 'fictive' swimming. In these neurones pressure on the cement gland evokes depolarising potentials, often with one or more spikes. 5. We propose that the stopping response depends on the excitation of pressure-sensitive trigeminal receptors which innervate the cement gland. These release an excitatory amino acid to excite brainstem GABAergic reticulospinal neurones, which inhibit spinal neurones to turn off the central pattern generator for swimming. There may also be a less direct pathway.

The Action of Acetylcholine on the Locomotor Central Pattern Generator for Swimming in Xenopus Embryos

The Action of Acetylcholine on the Locomotor Central Pattern Generator for Swimming in <i>Xenopus</i> Embryos