In Vivo Electrophysiology of Peptidergic Neurons in Deep Layers of the Lumbar Spinal Cord after Optogenetic Stimulation of Hypothalamic Paraventricular Oxytocin Neurons in Rats.

Published on Mar 26, 2021in International Journal of Molecular Sciences4.556
· DOI :10.3390/IJMS22073400
Daisuke Uta10
Estimated H-index: 10
,
Takumi Oti6
Estimated H-index: 6
+ 1 AuthorsHirotaka Sakamoto28
Estimated H-index: 28
Source
Abstract
The spinal ejaculation generator (SEG) is located in the central gray (lamina X) of the rat lumbar spinal cord and plays a pivotal role in the ejaculatory reflex. We recently reported that SEG neurons express the oxytocin receptor and are activated by oxytocin projections from the paraventricular nucleus of hypothalamus (PVH). However, it is unknown whether the SEG responds to oxytocin in vivo. In this study, we analyzed the characteristics of the brain–spinal cord neural circuit that controls male sexual function using a newly developed in vivo electrophysiological technique. Optogenetic stimulation of the PVH of rats expressing channel rhodopsin under the oxytocin receptor promoter increased the spontaneous firing of most lamina X SEG neurons. This is the first demonstration of the in vivo electrical response from the deeper (lamina X) neurons in the spinal cord. Furthermore, we succeeded in the in vivo whole-cell recordings of lamina X neurons. In vivo whole-cell recordings may reveal the features of lamina X SEG neurons, including differences in neurotransmitters and response to stimulation. Taken together, these results suggest that in vivo electrophysiological stimulation can elucidate the neurophysiological response of a variety of spinal neurons during male sexual behavior.
References31
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#1Takumi Oti (Kanagawa University)H-Index: 6
#2Keita Satoh (Okayama University)H-Index: 7
Last. Hirotaka Sakamoto (University of Oxford)H-Index: 28
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Summary Oxytocinergic neurons in the paraventricular nucleus of the hypothalamus that project to extrahypothalamic brain areas and the lumbar spinal cord play an important role in the control of erectile function and male sexual behavior in mammals. The gastrin-releasing peptide (GRP) system in the lumbosacral spinal cord is an important component of the neural circuits that control penile reflexes in rats, circuits that are commonly referred to as the “spinal ejaculation generator (SEG).” We ha...
3 CitationsSource
#1Daisuke UtaH-Index: 10
#2Kohei KogaH-Index: 21
Last. Megumu YoshimuraH-Index: 40
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BACKGROUND Although the widely used single L-enantiomers of local anesthetics have less toxic effects on the cardiovascular and central nervous systems, the mechanisms mediating their antinociceptive actions are not well understood. The authors hypothesized that significant differences in the ion channel blocking abilities of the enantiomers of bupivacaine would be identified. METHODS The authors performed electrophysiologic analysis on rat dorsal root ganglion neurons in vitro and on spinal tra...
1 CitationsSource
#1Norikazu Kiguchi (Wakayama Medical University)H-Index: 24
#2Daisuke Uta (University of Toyama)H-Index: 10
Last. Shiroh Kishioka (Wakayama Medical University)H-Index: 27
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Abstract Gastrin-releasing peptide (GRP) receptor-expressing (GRPR)+ neurons have a central role in the spinal transmission of itch. Because their fundamental regulatory mechanisms are not yet understood, it is important to determine how such neurons are excited and integrate itch sensations. In this study, we investigated the mechanisms for the activation of itch-responsive GRPR+ neurons in the spinal dorsal horn (SDH). GRPR+ neurons expressed the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic...
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Functional properties of lamina X neurons in the spinal cord remain unknown despite the established role of this area for somatosensory integration, visceral nociception, autonomic regulation, and motoneuron output modulation. Investigations of neuronal functioning in the lamina X have been hampered by technical challenges. Here we introduce an ex-vivo spinal cord preparation with both dorsal and ventral roots still attached for functional studies of the lamina X neurons and their connectivity u...
7 CitationsSource
Oxytocin (OT) is released into the brain from the cell soma, axons, and dendrites of neurosecretory cells in the hypothalamus. Locally released OT can activate OT receptors, form inositol-1,4,5-trisphosphate and elevate intracellular free calcium (Ca2+) concentrations [(Ca2+)i] in self and neighboring neurons in the hypothalamus, resulting in further OT release: i.e., autocrine or paracrine systems of OT-induced OT release. CD38-dependent cyclic ADP-ribose (cADPR) is also involved in this autore...
28 CitationsSource
#1Susan A. Deuchars (University of Leeds)H-Index: 19
#2Varinder K. Lall (University of Leeds)H-Index: 6
The sympathetic nervous system comprises one half of the autonomic nervous system and participates in maintaining homeostasis and enabling organisms to respond in an appropriate manner to perturbations in their environment, either internal or external. The sympathetic preganglionic neurons (SPNs) lie within the spinal cord and their axons traverse the ventral horn to exit in ventral roots where they form synapses onto postganglionic neurons. Thus, these neurons are the last point at which the ce...
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Lower spinal cord injuries frequently cause sexual dysfunction in men, including erectile dysfunction and an ejaculation disorder. This indicates that the important neural centers for male sexual function are located within the lower spinal cord. It is interesting that the lumbar spinal segments contain several neural circuits, showing a clear sexually dimorphism that, in association with neural circuits of the thoracic and sacral spinal cord, are critical in expressing penile reflexes during se...
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#1Natalie Kozyrev (UM: University of Michigan)H-Index: 2
#2Michael N. Lehman (UM: University of Michigan)H-Index: 53
Last. Lique M. Coolen (UM: University of Michigan)H-Index: 45
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ABSTRACT Introduction Ejaculation is a complex reflex mediated by a spinal ejaculation generator located in the lumbosacral spinal cord and consisting of a population of lumbar spinothalamic (LSt) neurons. LSt neurons and their intraspinal axonal projections contain several neuropeptides, including gastrin‐releasing peptide (GRP). Aim To test the hypothesis that GRP is critically involved in mediating ejaculation by acting in autonomic and motor areas of the lumbosacral spinal cord, utilizing a ...
22 CitationsSource
#1Hirotaka Sakamoto (Kyoto Prefectural University of Medicine)H-Index: 28
#2Ken-ichi Matsuda (Kyoto Prefectural University of Medicine)H-Index: 27
Last. Mitsuhiro Kawata (Kyoto Prefectural University of Medicine)H-Index: 41
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Neurons in the upper lumbar spinal cord project axons containing gastrin-releasing peptide (GRP) to innervate lower lumbar regions controlling erection and ejaculation. This system is vestigial in female rats and in males with genetic dysfunction of androgen receptors, but in male rats, pharmacological stimulation of spinal GRP receptors restores penile reflexes and ejaculation after castration. GRP offers new avenues for understanding potential therapeutic approaches to masculine reproductive d...
87 CitationsSource
During acute and chronic inflammation visceral pain perception is altered. Conflicting data exist, however, on visceral pain perception in the postinflammatory phase. The aim of the present study was to investigate whether visceral pain perception is altered after resolution of dextran sodium sulfate (DSS)-induced inflammation of the colon. Visceral sensory function in mice was assessed by monitoring behavioral responses to intracolonic capsaicin instillation. Two hours later the number of c-Fos...
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