Kinematic and electromyographic analysis of the functional role of the body axis during terrestrial and aquatic locomotion in the salamander ambystoma tigrinum
01 Jan 1992-The Journal of Experimental Biology (The Company of Biologists Ltd)-Vol. 162, Iss: 1, pp 107-130
TL;DR: The transition from a traveling axial wave during swimming to a standing axialWave during trotting in A. tigrinum may be an appropriate analogy for similar transitions in axial locomotor function during the original evolution of terrestriality in early tetrapods.
Abstract: Summary Aquatic neotenic and terrestrial metamorphosed salamanders {Ambystoma tigrinum) were videotaped simultaneously with electromyographic (EMG) recording from five epaxial myotomes along the animal's trunk during swimming in a flow tank and trotting on a treadmill to investigate axial function during aquatic and terrestrial locomotion. Neotenic and metamorphosed individuals swim using very similar axial wave patterns, despite significant differences in axial morphology. During swimming, both forms exhibit traveling waves of axial flexion and muscle activity, with an increasing EMG-mechanical delay as these waves travel down the trunk. In contrast to swimming, during trotting metamorphosed individuals exhibit a standing wave of axial flexion produced by synchronous activation of ipsilateral epaxial myotomes along the trunk. Thus, metamorphosed individuals employ two distinct axial motor programs - one used during swimming and one used during trotting. The transition from a traveling axial wave during swimming to a standing axial wave during trotting in A. tigrinum may be an appropriate analogy for similar transitions in axial locomotor function during the original evolution of terrestriality in early tetrapods.
Citations
More filters
TL;DR: The design of a neural circuit that has a general organization corresponding to that hypothesized by neurobiologists is presented, based on a body central pattern generator corresponding to a lamprey-like swimming controller, and is extended with a limb CPG for controlling the salamander's limbs.
Abstract: This article investigates the neural mechanisms underlying salamander locomotion, and develops a biologically plausible connectionist model of a central pattern generator capable of producing the typical aquatic and terrestrial gaits of the salamander. It investigates, in particular, what type of neural circuitry can produce and modulate the two locomotor programs identified within the salamander's spinal cord; namely, a traveling wave of neural activity for swimming and a standing wave for trotting. A two-dimensional biomechanical simulation of the salamander's body is developed whose muscle contraction is determined by the locomotion controller simulated as a leaky-integrator neural network. While the connectivity of the neural circuitry underlying locomotion in the salamander has not been decoded for the moment, this article presents the design of a neural circuit that has a general organization corresponding to that hypothesized by neurobiologists. In particular, the locomotion controller is based on a body central pattern generator (CPG) corresponding to a lamprey-like swimming controller, and is extended with a limb CPG for controlling the salamander's limbs. The complete controller is developed in three stages: first the development of segmental oscillators, second the development of intersegmental coupling for the making of a lamprey-like swimming CPG, and finally the development of the limb CPG and its coupling to the body CPG. A genetic algorithm is used to determine the parameters of the neural circuit for the different stages, given a high-level description of the desired state space trajectories of the different subnetworks. A controller is thus developed that can produce neural activities and locomotion gaits very similar to those observed in the real salamander. By varying the tonic (i.e. non-oscillating) excitation applied to the network, the speed, direction and type of gait can be varied.
355 citations
Cites background or methods from "Kinematic and electromyographic ana..."
...…the tonic input (speeds varyingfrom 0.0 to 0.45m/s when the input varies from 0.2 to 1.3).cies compared to the swimming frequencies observed inreal salamanders (Frolich & Biewener, 1992; Delvolv eet al., 1997).7Turning can be induced by applying asymmetricalinput between left and right (Figure 10)....
[...]
...Simulations show that, when modulated by di erentsignals from the brain stem, our proposed locomotorcircuit is capable of producing the two distinct motorprograms measured by EMG recordings during swim-ming and trotting (Frolich & Biewener, 1992; Delvolv eet al., 1997)....
[...]
...…are then out of phase, while diagonal limbs are inphase.1 EMG recordings have shown that two di er-ent motor programs underly these typical gaits, with atraveling of neural activity for swimming and a mainlystanding wave during trotting (Frolich & Biewener,1992; Delvolv e et al., 1997)....
[...]
...…byexcitatory bathes in spinal preparations of newts (Del-volv e et al., 1999).12 Neural waves with a wave-length corresponding to approximately the length ofthe body have also been measured by EMG recordingsduring swimming in salamander (Frolich & Biewener,1992) and newt (Delvolv e et al., 1997)....
[...]
...…and, in particular, the synchrony of all segmentsof the trunk are very similar to EMG recordings duringtrotting in the real salamander (Frolich & Biewener,1992; Delvolv e et al., 1997).6 Table 7 gives the connec-tivity of the limb CPG and its projections to the limbmotoneurons and the…...
[...]
TL;DR: The term “locomotor module” is introduced to identify anatomical subregions of the musculoskeletal system that are highly integrated and act as functional units during locomotion and has produced the diverse locomotor abilities of modern birds.
Abstract: The evolution of avian flight can be interpreted by analyzing the sequence of modifications of the primitive tetrapod locomotor system through time. Herein, we introduce the term "locomotor module" to identify anatomical subregions of the musculoskeletal system that are highly integrated and act as functional units during locomotion. The first tetrapods, which employed lateral undulations of the entire body and appendages, had one large locomotor module. Basal dinosaurs and theropods were bipedal and possessed a smaller locomotor module consisting of the hind limb and tail. Bird flight evolved as the superimposition of a second (aerial) locomotor capability onto the ancestral (terrestrial) theropod body plan. Although the origin of the wing module was the primary innovation, alterations in the terrestrial system were also significant. We propose that the primitive theropod locomotor module was functionally and anatomically subdivided into separate pelvic and caudal locomotor modules. This decoupling freed the tail to attain a new and intimate affiliation with the forelimb during flight, a configuration unique to birds. Thus, the evolution of flight can be viewed as the origin and novel association of locomotor modules. Differential elaboration of these modules in various lineages has produced the diverse locomotor abilities of modern birds.
223 citations
01 Oct 1993-Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology
TL;DR: Midline kinematics with synchronized electromyograms from the red and white muscles on both sides of bluegill sunfish (Lepomis macrochirus) during escape behaviors which were elicited from fish both at a standstill and during steady speed swimming were quantified.
Abstract: We quantified midline kinematics with synchronized electromyograms (emgs) from the red and white muscles on both sides of bluegill sunfish (Lepomis macrochirus) during escape behaviors which were elicited from fish both at a standstill and during steady speed swimming. Analyses of variance determined whether or not kinematic and emg variables differed significantly between muscle fiber types, among longitudinal positions, and between swimming versus standstill trials.
191 citations
Cites background from "Kinematic and electromyographic ana..."
...Furthermore a recent electromyographic study of salamanders (Frolich and Biewener 1992) found the general vertebrate pattern of swimming muscle activity which is posterior propagation....
[...]
...…studies of the steady undulatory swimming of a wide variety of vertebrates (eels: Grillner and Kashin 1976; trout: Williams et al. 1989; salamanders: Frolich and Biewener 1992; snakes: Jayne 1988) have also found that the rate of propagation of muscle activity exceeds that of the kinematic events....
[...]
TL;DR: Comparisons with animal data are presented, and the results show striking similarities with the gaits observed with real salamanders, in particular concerning the timing of the body’s and limbs’ movements and the relative speed of locomotion.
Abstract: In this paper, we present Salamandra robotica II: an amphibious salamander robot that is able to walk and swim. The robot has four legs and an actuated spine that allow it to perform anguilliform swimming in water and walking on the ground. The paper first presents the new robot hardware design, which is an improved version of Salamandra robotica I. We then address several questions related to body–limb coordination in robots and animals that have a sprawling posture like salamanders and lizards, as opposed to the erect posture of mammals (e.g., in cats and dogs). In particular, we investigate how the speed of locomotion and curvature of turning motions depend on various gait parameters such as the body–limb coordination, the type of body undulation (offset, amplitude, and phase lag of body oscillations), and the frequency. Comparisons with animal data are presented, and our results show striking similarities with the gaits observed with real salamanders, in particular concerning the timing of the body’s and limbs’ movements and the relative speed of locomotion.
187 citations
TL;DR: The goal of the project is to use robots as tools for gaining a better understanding of locomotion control in vertebrates and to develop new robot and control technologies for developing agile and adaptive outdoor robots.
Abstract: 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 control.
178 citations
Cites background from "Kinematic and electromyographic ana..."
...On ground, the salamander switches to a stepping gait, with the body making S-shaped standing waves with nodes at the girdles (Frolich and Biewener, 1992; Delvolvé et al., 1997)....
[...]
...EMG recordings (Frolich and Biewener, 1992; Delvolvé et al., 1997) and kinematic studies (Ashley-Ross and Bechtel, 2004) have confirmed the bimodal nature of salamander locomotion, with axial travelling waves along the body for swimming and mainly standing waves coordinated with the limbs for walking (Fig....
[...]
...EMG recordings (Frolich and Biewener, 1992; Delvolvé et al., 1997) and kinematic studies (Ashley-Ross and Bechtel, 2004) have confirmed the bimodal nature of salamander locomotion, with axial travelling waves along the body for swimming and mainly standing waves coordinated with the limbs for…...
[...]
..., the body produces one complete wave) and does not vary with the frequency of oscillation (Frolich and Biewener, 1992; Delvolvé et al., 1997)....
[...]
...There is a large amount of data available characterizing the kinematics of salamander locomotion, including axial movements (Edwards, 1976; Frolich and Biewener, 1992; Carrier, 1993; Delvolvé et al., 1997; Gillis, 1997; Ashley-Ross and Bechtel, 2004), hindlimb kinematics (Ashley-Ross, 1994a, b),…...
[...]
References
More filters
Book•
01 Jan 1976
TL;DR: This book reviews biological structural materials and systems and their mechanically important features and demonstrates that function at any particular level of biological integration is permitted and controlled by structure at lower levels of integration.
Abstract: This book deals with an interface between mechanical engineering and biology. Available for the first time in paperback, it reviews biological structural materials and systems and their mechanically important features and demonstrates that function at any particular level of biological integration is permitted and controlled by structure at lower levels of integration. Five chapters discuss the properties of materials in general and those of biomaterials in particular. The authors examine the design of skeletal elements and discuss animal and plant systems in terms of mechanical design. In a concluding chapter they investigate organisms in their environments and the insights gained from study of the mechanical aspects of their lives.
1,407 citations
TL;DR: This chapter deals with one limited aspect: how the central pattern generators that control locomotion function, and what directions seem most promising for gaining insight into how the eNS controls behavior.
Abstract: There is a gap to be bridged in vertebrate neurobiology, a gap between our knowledge of cellular mechanisms and behavior. We have achieved a widely expanded knowledge of how individual neurons function, and about synaptic transmission and membrane channels. We also increasingly understand the overall organization of different patterns of behavior, which principles apply, and which parts of eNS are important. We know much about how cells in the visual cortex respond, but little about how we perceive visual images; we know much about neuronal activity in motor cortex in relation to hand move ments, but little about how they are actually generated. One great challenge is to bridge this gap to understand how individual eNS neurons interact to generate different patterns of behavior, or make us perceive the environment, or memorize what we experience. Invertebrate neurobiologists have had considerable success in describing somc vcry important aspects of the cellular bases of behavior, such as asso ciative learning in molluscs (Kandel & Schwartz 1982) and basic patterns of behavior (Getting 1983a, Bullock 1982). In this chapter we deal with one limited aspect: how the central pattern generators that control locomotion function. Although the review is general, it emphasizes the vertebrates. We try to outline not only what we know, but also what directions seem most promising for gaining insight into how the eNS controls behavior. 233
779 citations
Book•
01 Jan 1929
TL;DR: It is hard to understand why the same method which has proved so suggestive in comparative anatomy has not been pursued more vigorously by embryologists, in order to elucidate the meaning of neurological structures, since this method is even more accessible to professed zoologists than to human anatomists in England.
Abstract: THE anatomy into which behaviour does not enter, at least unconsciously, is generally regarded as an academic study incapable of formulating general conclusions and therefore sterile. The anatomical method which has proved most valuable in the hands of British investigators is that which seeks to establish a comparative correlation between structure and function. It is therefore hard to understand why the same method which has proved so suggestive in comparative anatomy has not been pursued more vigorously by embryologists, in order to elucidate the meaning of neurological structures, since this method is even more accessible to professed zoologists than to human anatomists in England. Dr. Coghill, the author of these three lectures, is a member of the Wistar Institute of Anatomy and Biology at Philadelphia; but the lectures were delivered in London. He has made a parallel study of the development of behaviour and of the nervous system of Amblystoma with signal success for his purpose.Anatomy and the Problem of Behaviour.By G. E. Coghill. (Lectures delivered at University College, London.) Pp. xii + 113. (Cambridge: At the University Press, 1929.) 7s. 6d. net.
489 citations