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Postnatal Excitability Development and Innervation by Functional Transient Receptor Potential Vanilloid 1 (TRPV1) Terminals in Neurons of the Rat Spinal Sacral Dorsal Commissural Nucleus: an Electrophysiological Study

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Abstract

The sacral dorsal commissural nucleus (SDCN) in the spinal cord receives both somatic and visceral primary afferents. Transient receptor potential vanilloid 1 (TRPV1) channels are preferentially expressed in certain fine primary afferents. However, knowledge of the SDCN neurons postnatal excitability development and their contacts with TRPV1 fibers remains elusive. Here, whole-cell recordings were conducted in spinal cord slices to evaluate the postnatal development of SDCN neurons and their possible contacts with functional TRPV1-expressing terminals. SDCN neurons in neonatal (postnatal day (P) 1–2), young (P8-10), and adult rats (P35-40) have different electrophysiological properties. SDCN neurons in neonatal rats have higher frequency of spontaneous firing, higher resting membrane potential, and lower presynaptic glutamate release probability. However, no difference in quantal release was found. At all developmental stages, TRPV1 activation with the selective agonist capsaicin increases glutamate release in the presence of tetrodotoxin, which blocks action potential-dependent and polysynaptic neurotransmission, indicating that functional TRPV1 fibers innervate SDCN neurons directly. Capsaicin-induced presynaptic glutamate release onto SDCN neurons depends on external Ca2+ influx through TRPV1 channels; voltage-dependent calcium channels had a slighter impact. In contrast, capsaicin blocked C fiber-evoked synaptic transmission, indicating that TRPV1 activation has opposite effects on spontaneous asynchronous and action potential-dependent synchronous glutamate release. These data indicate that excitability of SDCN neurons undergoes a developmental shift, and these neurons receive functional TRPV1 terminals from early postnatal stage. The opposite action of capsaicin on asynchronous and synchronous glutamate release should be taken into account when TRPV1 channels are considered as therapeutic targets.

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Acknowledgments

The author thanks Professor Scott M. Thompson (Department of Physiology, University of Maryland School of Medicine, Baltimore, MD 21201, USA) for his supports on this project. This work was supported in part by the National Natural Science Foundation of China (No. 30000052) and Jiangsu University Grant (K.Y.).

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Authors and Affiliations

  1. School of Medicine and Affiliated Hospital Electrophysiology Laboratory, Jiangsu University, Zhenjiang, Jiangsu, 212013, China

    Kun Yang

  2. Department of Physiology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA

    Kun Yang

  3. Department of Neurology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA

    Kun Yang

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Correspondence to Kun Yang.

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All experiments conformed to the US National Institutes of Health Guide to the Care and Use of Laboratory Animals and were approved by the University of Maryland School of Medicine and Jiangsu University Institutional Animal Care and Use Committees.

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The author declares that he has no competing interests.

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Yang, K. Postnatal Excitability Development and Innervation by Functional Transient Receptor Potential Vanilloid 1 (TRPV1) Terminals in Neurons of the Rat Spinal Sacral Dorsal Commissural Nucleus: an Electrophysiological Study. Mol Neurobiol 53, 6033–6042 (2016). https://doi.org/10.1007/s12035-015-9510-x

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  • DOI: https://doi.org/10.1007/s12035-015-9510-x

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