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bioRxiv · 10.1101/2020.05.05.078444

Direct evidence for decreased presynaptic inhibition evoked by PBSt group I muscle afferents after chronic SCI and recovery with step-training in the decerebrated rat

Caron, G.·Bilchak, J. N.·Cote, M.-P.
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Abstract

Spinal cord injury (SCI) results in the disruption of supraspinal control of spinal networks and an increase in the relative influence of afferent feedback to sublesional neural networks, both of which contribute to enhancing spinal reflex excitability. Hyperreflexia occurs in ~75% of individuals with chronic SCI and critically hinders functional recovery and quality of life. It is suggested to result from an increase in motoneuronal excitability and a decrease in presynaptic and postsynaptic inhibitory mechanisms. In contrast, locomotor training decreases hyperreflexia by restoring presynaptic inhibition. Primary afferent depolarization (PAD) is a powerful presynaptic inhibitory mechanism that selectively gates primary afferent transmission to spinal neurons to adjust reflex excitability and ensure smooth movement. However, the effect of chronic SCI and step-training on the reorganization of presynaptic inhibition evoked by hindlimb afferents, and the contribution of PAD has never been demonstrated. The objective of this study is to directly measure changes in presynaptic inhibition through dorsal root potentials (DRPs) and its association to plantar H-reflex inhibition. We provide direct evidence that H-reflex hyperexcitability is associated with a decrease in transmission of PAD pathways activated by PBSt afferents after chronic SCI. More precisely, we illustrate that PBSt group I muscle afferents evoke a similar pattern of inhibition onto both L4-DRPs and plantar H-reflexes evoked by the tibial nerve in Control and step-trained animals, but not in chronic SCI rats. These changes are not observed after step-training, suggesting a role for activity-dependent plasticity to regulate PAD pathways activated by flexor muscle group I afferents. Key point summaryO_LIPresynaptic inhibition is modulated by supraspinal centers and primary afferents in order to filter sensory information, adjust spinal reflex excitability, and ensure smooth movements. C_LIO_LIAfter SCI, the supraspinal control of primary afferent depolarization (PAD) interneurons is disengaged, suggesting an increased role for sensory afferents. While increased H-reflex excitability in spastic individuals indicates a possible decrease in presynaptic inhibition, it remains unclear whether a decrease in sensory-evoked PAD contributes to this effect. C_LIO_LIWe investigated whether the PAD evoked by hindlimb afferents contributes to the change in presynaptic inhibition of the H-reflex in a decerebrated rat preparation. We found that chronic SCI decreases presynaptic inhibition of the plantar H-reflex through a reduction in PAD evoked by PBSt muscle group I afferents. C_LIO_LIWe further found that step-training restored presynaptic inhibition of the plantar H-reflex evoked by PBSt, suggesting the presence of activity-dependent plasticity of PAD pathways activated by flexor muscle group I afferents. C_LI

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Caron, G., Bilchak, J. N., Cote, M.-P.. 2020-05-05. Direct evidence for decreased presynaptic inhibition evoked by PBSt group I muscle afferents after chronic SCI and recovery with step-training in the decerebrated rat. https://doi.org/10.1101/2020.05.05.078444

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