Balancing central control and sensory feedback produces adaptable and robust locomotor patterns in a spiking, neuromechanical 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, namely stretch 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 replicates locomotor patterns observed in-vitro and in-vivo for swimming and trotting gaits. Additionally, a modular descending reticulospinal drive to the central pattern generation network allows to accurately control the activation, frequency and phase relationship of the different sections of the limb and axial circuits. In closed-loop swimming simulations (i.e. including axial stretch feedback), systematic evaluations reveal that intermediate values of feedback strength increase the tail beat frequency and reduce the intersegmental phase lag, contributing to a more coordinated, faster and energy-efficient locomotion. Interestingly, the result is conserved across different feedback topologies (ascending or descending, excitatory or inhibitory), suggesting that it may be an inherent property of axial proprioception. Moreover, intermediate feedback strengths expand the stability region of the network, enhancing its tolerance to a wider range of descending drives, internal parameters’ modifications and noise levels. Conversely, high values of feedback strength lead to a loss of controllability of the network and a degradation of its locomotor performance. Overall, this study highlights the beneficial role of proprioception in generating, modulating and stabilizing locomotion patterns, provided that it does not excessively override centrally-generated locomotor rhythms. This work also underscores the critical role of detailed, biologically-realistic neural networks to improve our understanding of vertebrate locomotion. Author summary In 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.

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