Journal
JOURNAL OF NEUROSCIENCE
Volume 43, Issue 18, Pages 3245-3258Publisher
SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.1897-22.2023
Keywords
dorsal horn; dorsal root potentials; marginal zone; nociception; presynaptic inhibition; primary afferents
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Mirror-image pain arises from pathologic alterations in the nociceptive processing network that controls functional lateralization of the primary afferent input. Our study reveals that decussating primary afferent branches reach contralateral Lamina I, where neurons receive excitatory drive from the contralateral fibers and also ipsilateral input, implying their involvement in bilateral information processing. The contralateral fiber input is under inhibitory control, and a pathological disinhibition of the decussating pathways can contribute to induction of hypersensitivity and mirror-image pain.
Mirror-image pain arises from pathologic alterations in the nociceptive processing network that controls functional lateraliza-tion of the primary afferent input. Although a number of clinical syndromes related to dysfunction of the lumbar afferent system are associated with the mirror-image pain, its morphophysiological substrate and mechanism of induction remain poorly understood. Therefore, we used ex vivo spinal cord preparation of young rats of both sexes to study organization and processing of the contralateral afferent input to the neurons in the major spinal nociceptive projection area Lamina I. We show that decussating primary afferent branches reach contralateral Lamina I, where 27% of neurons, including projection neurons, receive monosynaptic and/or polysynaptic excitatory drive from the contralateral AS-fibers and C-fibers. All these neurons also received ipsilateral input, implying their involvement in the bilateral information processing. Our data further show that the contralateral AS-fiber and C-fiber input is under diverse forms of inhibitory control. Attenuation of the affer-ent-driven presynaptic inhibition and/or disinhibition of the dorsal horn network increased the contralateral excitatory drive to Lamina I neurons and its ability to evoke action potentials. Furthermore, the contralateral APS-fibers presynaptically con-trol ipsilateral C-fiber input to Lamina I neurons. Thus, these results show that some lumbar Lamina I neurons are wired to the contralateral afferent system whose input, under normal conditions, is subject to inhibitory control. A pathologic disinhi-bition of the decussating pathways can open a gate controlling contralateral information flow to the nociceptive projection neurons and, thus, contribute to induction of hypersensitivity and mirror-image pain.
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