Sensory and central contributions to motor pattern generation in a spiking, neuro-mechanical model of the salamander spinal cord

Abstract This study introduces a novel neuromechanical model employing a detailed spiking neural network to explore the role of axial proprioceptive sensory feedback in salamander locomotion. Unlike previous studies that often oversimplified the dynamics of the locomotor networks, our model includes detailed simulations of the classes of neurons that are considered responsible for generating movement patterns. The locomotor circuits, modeled as a spiking neural network of adaptive leaky integrate-and-fire neurons, are coupled to a three-dimensional mechanical model of a salamander with realistic physical parameters and simulated muscles. In open-loop simulations (i.e., without sensory feedback) the model accurately replicates locomotor patterns observed in-vitro and in-vivo for swimming and trotting gaits. Additionally, a modular architecture of the descending reticulospinal (RS) drive to the central pattern generation (CPG) network, allows to accurately control the activation, frequency and phase relationship of the different sections of the limb and axial circuits. In closed-loop simulations (i.e. with the inclusion of axial proprioceptive sensory feedback), systematic evaluations reveal that intermediate values of feedback strength significantly enhance the locomotor efficiency and robustness to disturbances during swimming. Specifically, our results show that sensory feedback increases the tail beat frequency and reduces the intersegmental phase lag, contributing to more coordinated and faster movement patterns. Moreover, the presence of feedback expanded the stability region of the closed-loop swimming network, enhancing tolerance to a wider range of external stimulations, internal parameters’ modulation and noise levels. This study provides new insights into the complex interplay between central and peripheral pattern generation mechanisms, offering potential strategies for developing advanced biomimetic robots. Additionally, this study underscores the critical role of detailed, biologically-realistic neural networks to improve our understanding of vertebrate locomotion. Author summaryIn this paper, we developed a computational model to investigate how salamanders move, both while swimming and walking. Unlike previous studies that often oversimplified the dynamics of these complex neural networks, our model includes detailed simulations of the classes of neurons that are considered responsible for generating movement patterns. The locomotor circuits, modeled as a spiking neural network, are coupled to a three-dimensional mechanical model of a salamander with realistic physical parameters and simulated muscles. The neural model integrates axial proprioceptive sensory feedback from the body’s movements to modulate the locomotor gaits. Our simulations suggest that this sensory feedback plays a major role in controlling the rhythm and coordination of movements. This has implications for understanding not only how salamanders move but also provides insights into the evolution of locomotion in vertebrates. By investigating how central and sensory mechanisms interact to produce efficient and adaptable movement, our work contributes to the broader field of neuroscience and robotics, offering potential strategies for designing more effective biomimetic robots.