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Pressure overload changes mesenteric afferent nerve responses in a stress-dependent way in a fasting rat model

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Abstract

It is well known that overload changes the mechanical properties of biological tissues and fasting changes the responsiveness of intestinal afferents. This study aimed to characterize the effect of overload on mechanosensitivity in mesenteric afferent nerves in normal and fasted Sprague–Dawley rats. Food was restricted for 7 days in the Fasting group. Jejunal whole afferent nerve firing was recorded during three distensions, i.e., ramp distension to 80 cmH2O luminal pressure (D1), sustained distension to 120 cmH2O for 2 min (D2), and again to 80 cmH2O (D3). Multiunit afferent recordings were separated into low-threshold (LT) and wide-dynamic-range (WDR) single-unit activity for D1 and D3. Intestinal deformation (strain), distension load (stress), and firing frequency of mesenteric afferent nerve bundles [spike rate increase ratio (SRIR)] were compared at 20 cmH2O and 40 cmH2O and maximum pressure levels among distensions and groups. SRIR and stress changes showed the same pattern in all distensions. The SRIR and stress were larger in the Fasting group compared to the Control group (P < 0.01). SRIR was lower in D3 compared to D1 in controls (P < 0.05) and fasting rats (P < 0.01). Total single units and LT were significantly lower in Fasting group than in Controls at D3. LT was significantly higher in D3 than in D1 in Controls. Furthermore, correlation was found between SRIR with stress (R = 0.653, P < 0.001). In conclusion, overload decreased afferent mechanosensitivity in a stress-dependent way and was most pronounced in fasting rats. Fasting shifts LT to WDR and high pressure shifts WDR to LT in response to mechanical stimulation.

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Acknowledgements

The studies were financially supported by grants from Chongqing Science and Technology Commission (cstc2013kjrc-ljrccj10003), National “111 Plan” Base (B06023) and Danish Karen Elise Jensen Foundation (Grand No. 903959).

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All authors participated in the study design and contributed to the manuscript. LB conducted the animal experiments and analyzed the data with JZ. DL helped with the mechanical data analysis. LB drafted the manuscript that was revised by JZ and HG. HG designed the experiments and obtained the funding. All authors have read and approved the final version of the manuscript.

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Correspondence to Hans Gregersen.

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The authors declare that they have no conflict of interest.

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Bao, L., Zhao, J., Liao, D. et al. Pressure overload changes mesenteric afferent nerve responses in a stress-dependent way in a fasting rat model. Biomech Model Mechanobiol 19, 1741–1753 (2020). https://doi.org/10.1007/s10237-020-01305-8

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  • DOI: https://doi.org/10.1007/s10237-020-01305-8

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