Neuronal Control of Swimming Behavior: Comparison of Vertebrate and Invertebrate Model Systems

Swimming movements in the leech and lamprey are highly analogous, and lack homology. Thus, similarities in mechanisms must arise from convergent evolution rather than from common ancestry. Despite over 40 years of parallel investigations into this annelid and primitive vertebrate, a close comparison of the approaches and results of this research is lacking. The present review evaluates the neural mechanisms underlying swimming in these two animals and describes the many similarities that provide intriguing examples of convergent evolution. Specifically, we discuss swim initiation, maintenance and termination, isolated nervous system preparations, neural-circuitry, central oscillators, intersegmental coupling, phase lags, cycle periods and sensory feedback. Comparative studies between species highlight mechanisms that optimize behavior and allow us a broader understanding of nervous system function

Evolutionary Divergence in Developmental Strategies and Neuromodulatory Control Systems of Two Amphibian Locomotor Networks

Attempts to understand the neural mechanisms which produce behaviour must consider both prevailing sensory cues and the central cellular and synaptic changes they direct. At each level, neuromodulation can additionally shape the final output. We have investigated neuromodulation in the developing spinal motor networks in hatchling tadpoles of two closely related amphibians, Xenopus laevis and Rana temporaria to examine the subtle differences in their behaviours that could be attributed to their evolutionary divergence. At the point of hatching, both species can swim in response to a mechanosensory stimulus, however Rana embryos often display a more forceful, non-locomotory coiling behaviour. Whilst the synaptic drive that underlies these behaviours appears similar, subtle inter-specific differences in neuronal properties shape motor outputs in different ways. For example, Rana neurons express N-methyl-D-aspartate (NMDA)/serotonin (5-HT)-dependent oscillations, not present in hatchling Xenopus and many also exhibit a prominent slow spike after-hyperpolarisation. Such properties may endow the spinal circuitry of Rana with the ability to produce a more flexible range of outputs. Finally, we compare the roles of the neuromodulators 5-HT, noradrenaline (NA) and nitric oxide (NO) in shaping motor outputs. 5-HT increases burst durations during swimming in both Xenopus and Rana, but 5-HT dramatically slows the cycle period in Rana with little effect in Xenopus. Three distinct, but presumably homologous NO-containing brainstem clusters of neurons have been described, yet the effects of NO differ between species. In Xenopus, NO slows and shortens swimming in a manner similar to NA, yet in Rana NO and NA elicit the non-rhythmic coiling pattern

Evolutionary robotics and neuroscience

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Simulation and robotics studies of salamander locomotion: Applying neurobiological principles to the control of locomotion in robots

This article presents a project that aims at understanding the neural circuitry controlling salamander locomotion, and developing an amphibious salamander-like robot capable of replicating its bimodal locomotion, namely swimming and terrestrial walking. The controllers of the robot are central pattern generator models inspired by the salamander's locomotion control network. The goal of the project is twofold: (1) to use robots as tools for gaining a better understanding of locomotion control in vertebrates and (2) to develop new robot and control technologies for developing agile and adaptive outdoor robots. The article has four parts. We first describe the motivations behind the project. We then present neuromechanical simulation studies of locomotion control in salamanders. This is followed by a description of the current stage of the robotic developments. We conclude the article with a discussion on the usefulness of robots in neuroscience research with a special focus on locomotion contro

Design of artificial neural oscillatory circuits for the control of lamprey- and salamander-like locomotion using evolutionary algorithms

This dissertation investigates the evolutionary design of oscillatory artificial neural networks for the control of animal-like locomotion. It is inspired by the neural organ¬ isation of locomotor circuitries in vertebrates, and explores in particular the control of undulatory swimming and walking. The difficulty with designing such controllers is to find mechanisms which can transform commands concerning the direction and the speed of motion into the multiple rhythmic signals sent to the multiple actuators typically involved in animal-like locomotion. In vertebrates, such control mechanisms are provided by central pattern generators which are neural circuits capable of pro¬ ducing the patterns of oscillations necessary for locomotion without oscillatory input from higher control centres or from sensory feedback. This thesis explores the space of possible neural configurations for the control of undulatory locomotion, and addresses the problem of how biologically plausible neural controllers can be automatically generated.Evolutionary algorithms are used to design connectionist models of central pattern generators for the motion of simulated lampreys and salamanders. This work is inspired by Ekeberg's neuronal and mechanical simulation of the lamprey [Ekeberg 93]. The first part of the thesis consists of developing alternative neural controllers for a similar mechanical simulation. Using a genetic algorithm and an incremental approach, a variety of controllers other than the biological configuration are successfully developed which can control swimming with at least the same efficiency. The same method is then used to generate synaptic weights for a controller which has the observed biological connectivity in order to illustrate how the genetic algorithm could be used for developing neurobiological models. Biologically plausible controllers are evolved which better fit physiological observations than Ekeberg's hand-crafted model. Finally, in collaboration with Jerome Kodjabachian, swimming controllers are designed using a developmental encoding scheme, in which developmental programs are evolved which determine how neurons divide and get connected to each other on a two-dimensional substrate.The second part of this dissertation examines the control of salamander-like swimming and trotting. Salamanders swim like lampreys but, on the ground, they switch to a trotting gait in which the trunk performs a standing wave with the nodes at the girdles. Little is known about the locomotion circuitry of the salamander, but neurobiologists have hypothesised that it is based on a lamprey-like organisation. A mechanical sim¬ ulation of a salamander-like animat is developed, and neural controllers capable of exhibiting the two types of gaits are evolved. The controllers are made of two neural oscillators projecting to the limb motoneurons and to lamprey-like trunk circuitry. By modulating the tonic input applied to the networks, the type of gait, the speed and the direction of motion can be varied.By developing neural controllers for lamprey- and salamander-like locomotion, this thesis provides insights into the biological control of undulatory swimming and walking, and shows how evolutionary algorithms can be used for developing neurobiological models and for generating neural controllers for locomotion. Such a method could potentially be used for designing controllers for swimming or walking robots, for instance

Sensory Feedback Plays a Significant Role in Generating Walking Gait and in Gait Transition in Salamanders: A Simulation Study

Here, we investigate the role of sensory feedback in gait generation and transition by using a three-dimensional, neuro-musculo-mechanical model of a salamander with realistic physical parameters. Activation of limb and axial muscles were driven by neural output patterns obtained from a central pattern generator (CPG) which is composed of simulated spiking neurons with adaptation. The CPG consists of a body-CPG and four limb-CPGs that are interconnected via synapses both ipsilaterally and contralaterally. We use the model both with and without sensory modulation and four different combinations of ipsilateral and contralateral coupling between the limb-CPGs. We found that the proprioceptive sensory inputs are essential in obtaining a coordinated lateral sequence walking gait (walking). The sensory feedback includes the signals coming from the stretch receptor like intraspinal neurons located in the girdle regions and the limb stretch receptors residing in the hip and scapula regions of the salamander. On the other hand, walking trot gait (trotting) is more under central (CPG) influence compared to that of the peripheral or sensory feedback. We found that the gait transition from walking to trotting can be induced by increased activity of the descending drive coming from the mesencephalic locomotor region and is helped by the sensory inputs at the hip and scapula regions detecting the late stance phase. More neurophysiological experiments are required to identify the precise type of mechanoreceptors in the salamander and the neural mechanisms mediating the sensory modulation

Motor control in zebrafish : excitatory drive and developmental changes

An essential characteristic of human and animal life is the ability to move from one place to another, in order to survive in a complex environment. All the different forms of locomotion, like walking, swimming, crawling and flying, have one common feature: rhythmic and alternating movements of the body. These movements are generated by neuronal networks in the spinal cord. The overall aim of this thesis is to investigate the mechanisms underlying locomotion in zebrafish, with particular focus on excitatory drive and developmental changes. Excitatory interneurons are believed to represent the core components for the generation of the locomotor rhythm, since they drive both inhibitory interneurons and motoneurons. By ablating one specific group of interneurons, the V2a interneurons, we show that they represent an intrinsic source of excitation necessary for the normal expression of the locomotor rhythm. Ablation of V2a interneurons results in an increase in the threshold to induce swimming and a decrease in swimming frequency and episode duration. To demonstrate that the excitatory drive from ipsilateral premotor V2a interneurons is also sufficient to drive swimming, we used optogenetics to activate the V2a interneurons specifically. Upon illumination, V2a interneurons displayed rhythmic oscillations that resembled the typical beat-and-glide swimming. Peripheral nerve recordings confirmed that the bursting activity in single neurons corresponds to swimming activity, which is characterized by left-right-alternation and rostrocaudal delay. This indicates that swimming activity emerges from the activity of an underlying V2a interneuron network. The third aim of this thesis is to reveal the developmental changes of the swimming pattern and the motoneuron properties. By systematically recording peripheral nerve activity and primary motoneuron properties during different developmental stages, we were able to define the time frame of the switch in swimming behavior from larval episodic to adult continuous swimming to 4-5 weeks post fertilization. Primary motoneurons stop participating in swimming within the same time window and are from around 6 weeks onward only active during escape behavior. In conclusion, we show that the excitatory V2a interneurons in zebrafish are necessary and sufficient for the rhythm generating network to generate a coordinated swimming motor pattern and that there is a major switch in the locomotor pattern and primary motoneuron recruitment around 4-5 weeks of development

Evolution of swimming behaviors in nudibranch molluscs: A comparative analysis of neural circuitry

Behaviors are a product of underlying neural circuits, yet there is a paucity of mechanistic information about how nervous systems contribute to the repeated evolution of similar behaviors. Theoretical studies have predicted that the same behavioral output can be generated by neural circuits with different properties. Here, we test the theory in biological circuits by comparing the central pattern generator (CPG) circuits underlying swimming behaviors in nudibranchs (Mollusca, Gastropoda, Euthyneura, Nudipleura). In comparative studies of neural circuits, neurotransmitter content can serve as landmarks or molecular markers for neuron types. Here, we created a comprehensive map of GABA-immunoreactive neurons in six Nudipleura species. None of the known swim CPG neurons were GABA-ir, but they were located next to identifiable GABA-ir neurons/clusters. Despite strong conservation of the GABA-ergic system, there were differences, particularly in the buccal ganglia, which may represent adaptive changes. We applied our knowledge of neurotransmitter distribution along with morphological traits to identify the neuron type Si1 in Flabellina, a species that swims via whole body left-right (LR) flexions and in Tritonia, a dorsal-ventral (DV) swimming species. Si1 is a CPG member of the LR species Melibe, whereas its homologue in the LR species Dendronotus is not. In Flabellina, Si1 was part of the LR CPG and despite having similar synaptic connections as Flabellina and Melibe, Si1 in Tritonia was not part of its DV swim CPG. Side by side circuit comparison of Flabellina, Melibe and Dendronotus revealed different combinations of circuit architecture and modulation resulting in different circuit configurations for LR swimming. This includes differences in the role and activity pattern of Si1, sensitivity to curare and the effect of homologues of C2, a DV CPG neuron, on the LR motor pattern. These results collectively reveal three different circuit variations for generating the same behavior. It suggests that the neural substrate from which behaviors arise is phylogenetically constrained. While this neural substrate can be configured in multiple different ways to generate the same outcome, the possibilities are finite and, as seen here, similar structural and functional neural motifs are used in the evolution of these circuits