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Postcolitis Alterations in Nociceptive Properties of Neurons in the Rat Nucleus Raphe Magnus and Dorsal Raphe Nucleus

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Abstract

Dysfunction of the brain serotonergic system is thought to play a leading role in the pathogenesis of chronic abdominal pain and comorbid somatic hyperalgesia, which ail a significant portion of patients with gastrointestinal diseases, even in remission. However, specific changes in nociceptive properties of the serotonergic structures that can be initiated by organic pathology and persist after its resolution remain obscure. The aim of our neurophysiological study conducted on anesthetized rats, healthy and recovered from colitis, was to reveal postcolitis alterations in neuronal responses of the nucleus raphe magnus (RMg) and dorsal raphe nucleus (DR) to visceral (colorectal distension) and somatic (squeezing of the tail) noxious stimulation, which persist after the resolution of intestinal inflammation. It was shown that both nuclei contain different groups of nociceptive neurons: (1) excited only by colorectal distension (visceral); (2) activated only by tail pinch (somatic); (3) excited by both of these types of stimulation (general); (4) inhibited by either type of pain stimulation. In the RMg of postcolitis rats, the number of inhibited neurons was increased, while the total proportion of excited nociceptive neurons was reduced compared to healthy animals. Colorectal distension in postcolitis rats evoked enhanced inhibition of RMg neurons, whereas noxious stimulation of their tail unaffected by the pathology led to increased excitation of RMg selective somatic and general nociceptive cells. In the DR of postcolitis rats, the proportion of inhibited neurons was reduced, while the increased population of excited neurons contained less visceral and more somatic selective cells. This was accompanied by an enhancement of selective responses of the latter to somatic pain stimuli and an increase in nonselective excitation of DR neurons in response to visceral and somatic nociceptive signals. The revealed neuronal alterations in the RMg and DR may promote postcolitis dysfunction of these raphe nuclei in the endogenous control of visceral and somatic pain sensitivity.

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Funding

The study was supported by the Russian Science Foundation, project no. 23-25-00151, https://rscf.ru/project/23-25-00151/.

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Authors and Affiliations

  1. Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg, Russia

    B. M. Sushkevich, I. B. Sivachenko & O. A. Lyubashina

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  1. B. M. Sushkevich
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  2. I. B. Sivachenko
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  3. O. A. Lyubashina
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Contributions

Conceptualization and experimental design (O.A.L.), data collection (B.M.S., I.B.S.), data processing (B.M.S., I.B.S, O.A.L.), writing and editing the manuscript (B.M.S., I.B.S., O.A.L.).

Corresponding author

Correspondence to O. A. Lyubashina.

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COMPLIANCE WITH ETHICAL STANDARDS

All experimental procedures complied with the ethical standards approved by the legal acts of the Russian Federation, the principles of the Basel Declaration, and the recommendations of the Institutional Animal Care and Use Committee of the Pavlov Institute of Physiology of the Russian Academy of Sciences.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest related to the publication of this article.

Additional information

Translated by A. Polyanovsky

Russian Text © The Author(s), 2023, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2023, Vol. 59, No. 4, pp. 292–309https://doi.org/10.31857/S004445292304006X.

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Sushkevich, B.M., Sivachenko, I.B. & Lyubashina, O.A. Postcolitis Alterations in Nociceptive Properties of Neurons in the Rat Nucleus Raphe Magnus and Dorsal Raphe Nucleus. J Evol Biochem Phys 59, 1057–1076 (2023). https://doi.org/10.1134/S0022093023040051

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  • DOI: https://doi.org/10.1134/S0022093023040051

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