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Nociception induces a differential presynaptic modulation of the synaptic efficacy of nociceptive and proprioceptive joint afferents

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Abstract

A previous study has indicated that during the state of central sensitization induced by the intradermic injection of capsaicin, there is a gradual facilitation of the dorsal horn neuronal responses produced by stimulation of the high-threshold articular afferents that is counteracted by a concurrent increase of descending inhibitory actions. Since these changes occurred without significantly affecting the responses produced by stimulation of the low-threshold articular afferents, it was suggested that the capsaicin-induced descending inhibition included a preferential presynaptic modulation of the synaptic efficacy of the slow conducting nociceptive joint afferents (Ramírez-Morales et al., Exp Brain Res 237:1629–1641, 2019). The present study was aimed to investigate more directly the contribution of presynaptic mechanisms in this descending control. We found that in the barbiturate anesthetized cat, stimulation of the high-threshold myelinated afferents in the posterior articular nerve (PAN) produces primary afferent hyperpolarization (PAH) in the slow conducting (25–35 m/s) and primary afferent depolarization (PAD) in the fast conducting (40–50 m/s) articular fibers. During the state of central sensitization induced by capsaicin, there is a supraspinally mediated shift of the autogenic PAH to PAD that takes place in the slow conducting fibers, basically without affecting the autogenic PAD generated in the fast conducting afferents. It is suggested that the change of presynaptic facilitation to presynaptic inhibition induced by capsaicin on the slow articular afferents is part of an homeostatic process aimed to keep the nociceptive-induced neuronal activity within manageable limits while preserving the proprioceptive information required for proper control of movement.

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Acknowledgements

We would like to thank Drs. E. Jankowska and S. Glusman for their  comments to an earlier version of this paper, to C León for technical assistance and to E Rosales for her excellent secretarial support.

Funding

This work was partly supported CONACyT grants 50900 and 255548. AR was holder of a CONACyT fellowship for doctoral studies.

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  1. Department of Physiology, Biophysics and Neurosciences, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Mexico City, Mexico

    A. Ramírez-Morales, E. Hernández & P. Rudomin

  2. El Colegio Nacional, Mexico City, Mexico

    P. Rudomin

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  1. A. Ramírez-Morales
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  2. E. Hernández
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  3. P. Rudomin
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Correspondence to P. Rudomin.

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Ramírez-Morales, A., Hernández, E. & Rudomin, P. Nociception induces a differential presynaptic modulation of the synaptic efficacy of nociceptive and proprioceptive joint afferents. Exp Brain Res 239, 2375–2397 (2021). https://doi.org/10.1007/s00221-021-06140-6

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