Dataset Information

Proprioceptive feedback amplification restores effective locomotion in a neuromechanical model of lampreys with spinal injuries.

ABSTRACT: Spinal injuries in many vertebrates can result in partial or complete loss of locomotor ability. While mammals often experience permanent loss, some nonmammals, such as lampreys, can regain swimming function, though the exact mechanism is not well understood. One hypothesis is that amplified proprioceptive (body-sensing) feedback can allow an injured lamprey to regain functional swimming even if the descending signal is lost. This study employs a multiscale, integrative, computational model of an anguilliform swimmer fully coupled to a viscous, incompressible fluid and examines the effects of amplified feedback on swimming behavior. This represents a model that analyzes spinal injury recovery by combining a closed-loop neuromechanical model with sensory feedback coupled to a full Navier-Stokes model. Our results show that in some cases, feedback amplification below a spinal lesion is sufficient to partially or entirely restore effective swimming behavior.

SUBMITTER: Hamlet C

PROVIDER: S-EPMC10089168 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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Proprioceptive feedback amplification restores effective locomotion in a neuromechanical model of lampreys with spinal injuries.

Hamlet Christina C Fauci Lisa L Morgan Jennifer R JR Tytell Eric D ED

Proceedings of the National Academy of Sciences of the United States of America 20230310 11

Spinal injuries in many vertebrates can result in partial or complete loss of locomotor ability. While mammals often experience permanent loss, some nonmammals, such as lampreys, can regain swimming function, though the exact mechanism is not well understood. One hypothesis is that amplified proprioceptive (body-sensing) feedback can allow an injured lamprey to regain functional swimming even if the descending signal is lost. This study employs a multiscale, integrative, computational model of a ...[more]

PMID: 36897980

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Project description:Epidural electrical stimulation can restore limb motor function after spinal cord injury by reactivating the surviving neural circuits. In previous epidural electrical stimulation studies, single electrode sites and continuous tetanic stimulation have often been used. With this stimulation, the body is prone to declines in tolerance and locomotion coordination. In the present study, rat models of complete spinal cord injury were established by vertically cutting the spinal cord at the T8 level to eliminate disturbance from residual nerve fibers, and were then subjected to epidural electrical stimulation. The flexible extradural electrode had good anatomical topology and matched the shape of the spinal canal of the implanted segment. Simultaneously, the electrode stimulation site was able to be accurately applied to the L2-3 and S1 segments of the spinal cord. To evaluate the biocompatibility of the implanted epidural electrical stimulation electrodes, GFAP/Iba-1 double-labeled immunofluorescence staining was performed on the spinal cord below the electrodes at 7 days after the electrode implantation. Immunofluorescence results revealed no significant differences in the numbers or morphologies of microglia and astrocytes in the spinal cord after electrode implantation, and there was no activated Iba-1+ cell aggregation, indicating that the implant did not cause an inflammatory response in the spinal cord. Rat gait analysis showed that, at 3 days after surgery, gait became coordinated in rats with spinal cord injury under burst stimulation. The regained locomotion could clearly distinguish the support phase and the swing phase and dynamically adjust with the frequency of stimulus distribution. To evaluate the matching degree between the flexible epidural electrode (including three stimulation contacts), vertebral morphology, and the level of the epidural site of the stimulation electrode, micro-CT was used to scan the thoracolumbar vertebrae of rats before and after electrode implantation. Based on the experimental results of gait recovery using three-site stimulation electrodes at L2-3 and S1 combined with burst stimulation in a rat model of spinal cord injury, epidural electrical stimulation is a promising protocol that needs to be further explored. This study was approved by the Animal Ethics Committee of Chinese PLA General Hospital (approval No. 2019-X15-39) on April 19, 2019.

Project description: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.

Dataset Information

Proprioceptive feedback amplification restores effective locomotion in a neuromechanical model of lampreys with spinal injuries.

Publications

Proprioceptive feedback amplification restores effective locomotion in a neuromechanical model of lampreys with spinal injuries.

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