From lamprey to salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander

The evolutionary transition from water to land required new locomotor modes and corresponding adjustments of the spinal "central pattern generators" for locomotion. Salamanders resemble the first terrestrial tetrapods and represent a key animal for the study of these changes. Based on recent physiological data from salamanders, and previous work on the swimming, limbless lamprey, we present a model of the basic oscillatory network in the salamander spinal cord, the spinal segment. Model neurons are of the Hodgkin-Huxley type. Spinal hemisegments contain sparsely connected excitatory and inhibitory neuron populations, and are coupled to a contralateral hemisegment. The model yields a large range of experimental findings, especially the NMDA-induced oscillations observed in isolated axial hemisegments and segments of the salamander Pleurodeles waltlii. The model reproduces most of the effects of the blockade of AMPA synapses, glycinergic synapses, calcium-activated potassium current, persistent sodium current, and -current. Driving segments with a population of brainstem neurons yields fast oscillations in the in vivo swimming frequency range. A minimal modification to the conductances involved in burst-termination yields the slower stepping frequency range. Slow oscillators can impose their frequency on fast oscillators, as is likely the case during gait transitions from swimming to stepping. Our study shows that a lamprey-like network can potentially serve as a building block of axial and limb oscillators for swimming and stepping in salamanders.

A Salamander’s Flexible Spinal Network for Locomotion, Modeled at Two Levels of Abstraction

Andrej Bicanski, Auke Ijspeert, Jérémie Knüsel

Animals have to coordinate a large number of muscles in different ways to efficiently move at various speeds and in different and complex environments. This coordination is in large part based on central pattern generators (CPGs). These neural networks are capable of producing complex rhythmic patterns when activated and modulated by relatively simple control signals. Although the generation of particular gaits by CPGs has been successfully modeled at many levels of abstraction, the principles underlying the generation and selection of a diversity of patterns of coordination in a single neural network are still not well understood. The present work specifically addresses the flexibility of the spinal locomotor networks in salamanders. We compare an abstract oscillator model and a CPG network composed of integrate-and-fire neurons, according to their ability to account for different axial patterns of coordination, and in particular the transition in gait between swimming and stepping modes. The topology of the network is inspired by models of the lamprey CPG, complemented by additions based on experimental data from isolated spinal cords of salamanders. Oscillatory centers of the limbs are included in a way that preserves the flexibility of the axial network. Similarly to the selection of forward and backward swimming in lamprey models via different excitation to the first axial segment, we can account for the modification of the axial coordination pattern between swimming and forward stepping on land in the salamander model, via different uncoupled frequencies in limb versus axial oscillators (for the same level of excitation). These results transfer partially to a more realistic model based on formal spiking neurons, and we discuss the difference between the abstract oscillator model and the model built with formal spiking neurons.

Oxford University Press2013

Salamandra Robotica II: An Amphibious Robot to Study Salamander-Like Swimming and Walking Gaits

Alessandro Crespi, André Guignard, Auke Ijspeert, Konstantinos Karakasiliotis

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.

Ieee-Inst Electrical Electronics Engineers Inc2013

Emergence of robust self-organized undulatory swimming based on local hydrodynamic force sensing

Kyoichi Akiyama, Auke Ijspeert, Kamilo Andres Melo Becerra, Laura Isabel Paez Coy, Robin Thandiackal

Undulatory swimming represents an ideal behavior to investigate locomotion control and the role of the underlying central and peripheral components in the spinal cord. Many vertebrate swimmers have central pattern generators and local pressure-sensitive receptors that provide information about the surrounding fluid. However, it remains difficult to study experimentally how these sensors influence motor commands in these animals. Here, using a specifically designed robot that captures the essential components of the animal neuromechanical system and using simulations, we tested the hypothesis that sensed hydrodynamic pressure forces can entrain body actuation through local feedback loops. We found evidence that this peripheral mechanism leads to self-organized undulatory swimming by providing intersegmental coordination and body oscillations. Swimming can be redundantly induced by central mechanisms, and we show that, therefore, a combination of both central and peripheral mechanisms offers a higher robustness against neural disruptions than any of them alone, which potentially explains how some vertebrates retain locomotor capabilities after spinal cord lesions. These results broaden our understanding of animal locomotion and expand our knowledge for the design of robust and modular robots that physically interact with the environment.

AMER ASSOC ADVANCEMENT SCIENCE2021

A Salamander’s Flexible Spinal Network for Locomotion, Modeled at Two Levels of Abstraction

Andrej Bicanski, Auke Ijspeert, Jérémie Knüsel

Oxford University Press2013