Simulations of neuromuscular control in lamprey swimming

Ekeberg, Örjan; Grillner, Sten

doi:10.1098/rstb.1999.0441

Cited by 121 publications

(74 citation statements)

References 36 publications

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“…Because of the high complexity, mathematical modeling is essential for understanding mechanisms underlying neuronal information processing in the CNS. Taking animal locomotion as a tractable focus of study, a number of models have previously been developed, ranging from neuronal circuit models for CPGs (44)(45)(46)(47) and body-fluid interactions during swimming (35,48) to integrated neuromechanical models for locomotion (49)(50)(51). An ultimate goal is to have dynamical models that are simple and amenable not only to numerical simulations but also to analytical studies, and which are fully validated by experimental data, with demonstrated predictability under perturbed conditions.…”

Section: Discussionmentioning

confidence: 99%

Biological clockwork underlying adaptive rhythmic movements

Iwasaki

Friesen

2014

Proc. Natl. Acad. Sci. U.S.A.

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Owing to the complexity of neuronal circuits, precise mathematical descriptions of brain functions remain an elusive ambition. A more modest focus of many neuroscientists, central pattern generators, are more tractable neuronal circuits specialized to generate rhythmic movements, including locomotion. The relative simplicity and welldefined motor functions of these circuits provide an opportunity for uncovering fundamental principles of neuronal information processing. Here we present the culmination of mathematical analysis that captures the adaptive behaviors emerging from interactions between a central pattern generator, the body, and the physical environment during locomotion. The biologically realistic model describes the undulatory motions of swimming leeches with quantitative accuracy and, without further parameter tuning, predicts the sweeping changes in oscillation patterns of leeches undulating in air or swimming in high-viscosity fluid. The study demonstrates that central pattern generators are capable of adapting oscillations to the environment through sensory feedback, but without guidance from the brain.A long-term ambition in neuroscience is to generate a detailed, complete model of the human brain (1). Still ambitious, and certainly more realistic, is the aim to model components of vertebrate nervous systems. Most advanced in this arena are models based on the circuits underlying motor functions, such as rhythmic body movements during locomotion. These movements are generated by spinal neural oscillator circuits called central pattern generators (CPGs) (2, 3). The enormous number of neurons in the vertebrate central nervous system currently prevents analysis at the level of defined circuits between individual neurons. However, the simpler, accessible CPGs underlying locomotion in the invertebrates provide dynamically rich platforms amenable to detailed analysis that can lead to deep understanding of how neuronal circuits generate extremely robust and adaptive oscillatory behaviors. The leech CPG for undulatory swimming provides such a platform. The isolated nerve cord, with most (4, 5), a few (6, 7), or even a single segmental ganglion (8, 9), displays "fictive swimming," where the rhythmic motor pattern closely resembles that recorded in intact animals. Moreover, the leech continues to swim without the brain (10, 11), with the nerve cord severed in midbody (5), or with the body cut in half (7).Our study addresses the following question: How does the leech swimming system achieve its astonishing robustness and adaptability? A detailed explanation of the mechanisms underlying such complex phenomena requires mathematical modeling and analysis because a unidirectional sequence of cause-andeffect relationships alone cannot explain dynamical properties arising from multiple feedback loops. An obstacle in exploring the emergence of the functional properties from highly interconnected neuronal circuits through model-based analysis is the lack of biological realism (1). We, therefore, have focused on the...

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Section: Discussionmentioning

confidence: 99%

Biological clockwork underlying adaptive rhythmic movements

Iwasaki

Friesen

2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Each CPG spinal region exhibits its own oscillatory frequency, but could entrain the rostral or/and caudal segments, respectively. Work on the lamprey has elucidated the structure and function of CPGs and the rostrocaudal gradient of excitation and led to impressive computer simulations (Ekeberg & Grillner 1999). Although the real neuronal circuit of a CPG has not yet been demonstrated in the limbed vertebrates (tetrapods), Ijspeert (2001) has succeeded to simulate a salamander during undulation and legged locomotion, thus the hypothetical basis for action of CPGs during legged locomotion has become more clear (http://lslwww.epfl.ch/birg).…”

Section: Control Of the Vertebrate Motion Systems (A ) Central Pattermentioning

confidence: 99%

Legs evolved only at the end!

Fischer

Witte

2006

Phil. Trans. R. Soc. A.

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Talking about legged locomotion often evokes the idea that animals using such devices are perfectly adapted to this kind of motion and should be copied by robotics. The aim of this contribution is to show that the evolution of legs comes late in phylogeny, be it in arthropods or vertebrates. Neural control of legs in vertebrates has to deal with conservative arrangements 'invented' for axial locomotion of metameric organisms. The structure of this paper is to show the importance of axial driven propulsion in vertebrates without legs, with legs and only at the end how limbs move the body in eutherian mammals.

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“…The hydrodynamics of swimming has been the subject of a variety of studies for more than half a century from experimental (3-6), theoretical (7)(8)(9)(10)(11), and computational (12)(13)(14)(15)(16)(17)(18)(19) perspectives. Recently there has been growing interest in integrating these physical approaches with neurobiological models using coupled neuromechanical simulations (20) and biomimetic devices (21,22) to study developmental and evolutionary aspects of the problem. Indeed, when a dead fish is dragged through water it flutters and moves in a manner reminiscent of a live, swimming fish (23).…”

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Gait and speed selection in slender inertial swimmers

Gazzola

Argentina

Mahadevan

2015

Proc. Natl. Acad. Sci. U.S.A.

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Inertial swimmers use flexural movements to push water and generate thrust. We quantify this dynamical process for a slender body in a fluid by accounting for passive elasticity and hydrodynamics and active muscular force generation and proprioception. Our coupled elastohydrodynamic model takes the form of a nonlinear eigenvalue problem for the swimming speed and locomotion gait. The solution of this problem shows that swimmers use quantized resonant interactions with the fluid environment to enhance speed and efficiency. Thus, a fish is like an optimized diode that converts a prescribed alternating transverse motion to forward motion. Our results also allow for a broad comparative view of swimming locomotion and provide a mechanistic basis for the empirical relation linking the swimmer's speed U, length L, and tail beat frequency f, given by U=L ∼ f [Bainbridge R (1958) J Exp Biol 35:109-133]. Furthermore, we show that a simple form of proprioceptive sensory feedback, wherein local muscle activation is function of body curvature, suffices to drive elastic instabilities associated with thrust production and leads to a spontaneous swimming gait without the need for a central pattern generator. Taken together, our results provide a simple mechanistic view of swimming consistent with natural observations and suggest ways to engineer artificial swimmers for optimal performance.inertial swimming | gait selection | proprioception U nderstanding locomotory behavior requires that we integrate the neural control of muscular dynamics with the body mechanics of the organism as it interacts with the environment. Simultaneously, we must also account for sensory feedback from the environment and from the organism's sense of its own shape. However, translating these concepts to quantitative theories is challenging because of the variety of organism sizes and shapes and the complexity of their physical and biological environment. Therefore, investigations typically focus on specific organisms and try to glean principles that might be of broader relevance. In the context of terrestrial locomotion, recent experimental and theoretical work on the undulating worm Caenorhabditis elegans (1) shows that proprioceptive feedback suffices to coordinate undulatory motions. Complementing these studies, general theoretical models have explored the conditions under which coordinated crawling occurs in a coupled brain-body-environment system (2). These models explain observations in larvae of Drosophila melanogaster, showing how a sensorimotor coupling that links brain, body, and environment can robustly lead to crawling in a range of conditions.Translating these ideas to macroscopic aquatic locomotion, when inertia dominates viscous forces, is a formidable challenge owing to the presence of complex hydrodynamic nonlinearities, which must be coupled to body mechanics and neural dynamics of proprioceptive and sensory feedback. The hydrodynamics of swimming has been the subject of a variety of studies for more than half a century from experimen...

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Simulations of neuromuscular control in lamprey swimming

Cited by 121 publications

References 36 publications

Biological clockwork underlying adaptive rhythmic movements

Biological clockwork underlying adaptive rhythmic movements

Legs evolved only at the end!

Gait and speed selection in slender inertial swimmers

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