Presence of the N-methyl-d-aspartic acid R1 glutamatergic receptor subunit in the lumbosacral spinal cord of male rats

Gougis, Sylvette; Prud'homme, Marie-Jeanne; Rampin, Olivier

doi:10.1016/s0304-3940(02)00143-x

Cited by 16 publications

(10 citation statements)

References 18 publications

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“…Immunocytochemical studies have revealed that the superficial laminae of the rat spinal cord contain both NMDAR1 and AMPA GluR1-R4 glutamatergic receptor subtypes (Yung 1998;Kerr et al 1998). Sacral parasympathetic nucleus (SPN) neurons and pudendal motoneurons, retrogradely labeled from the pelvic nerve and perineal striated muscles respectively, exhibit NMDAR1 and GluR1-R3 immunoreactivity (Gougis et al 2002;Chambille and Rampin 2002). Furthermore, GluR1 and GluR2 subunits of AMPA receptors are distributed in the superficial laminae of L5-L6 spinal segments at which penile afferents terminate, and GluR4 subunits are most intensively expressed in the MPG .…”

Section: Introductionmentioning

confidence: 99%

Anatomical evidence for glutamatergic transmission in primary sensory neurons and onto postganglionic neurons controlling penile erection in rats: an ultrastructural study with neuronal tracing and immunocytochemistry

Aı̈oun

Rampin

2005

Cell Tissue Res

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In male rats, the dorsal penile nerve (DPN) conveys sensory information from the genitals to the lumbosacral spinal segments of the spinal cord. DPN is the afferent limb of a reflex loop that supports reflexive erections, and that includes a network of spinal interneurons and autonomic and somatic motoneurons to the penis and perineal striated muscles. Autonomic efferent pathways to the penis relay in the major pelvic ganglion (MPG). Glutamate (Glu) is a likely candidate as a neurotransmitter of reflexive erections. Both AMPA and NMDA glutamatergic receptor subunits are present in the lumbosacral spinal cord, and AMPA and NMDA receptor antagonists block reflexive erections. In the present study, we used tract-tracing experiments combined with immunohistochemical and immunocytochemical techniques to ascertain the presence of Glu at two different levels of the network controlling reflexive erections. DPN afferents were localized in the dorsal horn of the lumbosacral cord and displayed the characteristics of either C-fibers or Adelta fibers. DPN terminals (some of them glutamatergic) were mainly distributed in the medial edge of the dorsal horn in the L6 spinal segment. GluR1 subunits were present in some DPN afferents, suggesting that they could be autoreceptors. DPN fibers were also present in the MPG, as were Glu terminals and GluR4 subunits. The results reveal the presence of Glu in DPN fibers and terminals and suggest that both the spinal cord and the MPG use glutamatergic transmission to control reflexive erections.

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Section: Introductionmentioning

confidence: 99%

Anatomical evidence for glutamatergic transmission in primary sensory neurons and onto postganglionic neurons controlling penile erection in rats: an ultrastructural study with neuronal tracing and immunocytochemistry

Aı̈oun

Rampin

2005

Cell Tissue Res

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“…First, glutamate is present in the dorsal root ganglion cells innervating the bladder and rectum (15), and NMDA and AMPA glutamatergic receptor subtypes are present in the lumbosacral spinal cord, as revealed by immunohistochemistry (8,13) and by in situ hybridization (37). Second, on in vitro preparations, preganglionic neurons of the sacral parasympathetic nucleus are activated by stimulation of either short interneurons (2) or of the lateral funiculus or of the dorsal gray commissure (24,25) through AMPA and NMDA receptors.…”

Section: Discussionmentioning

confidence: 99%

“…Thus NMDA and AMPA-kainate receptors participate to the spinal control of pelvic organs. Anatomically, both AMPA receptors (8) and NMDA receptors (13) are present in the rat lumbosacral spinal cord. In the present study, we tested the hypothesis that glutamate participates to the activation of the spinal proerectile network through NMDA and AMPA glutamatergic receptors.…”

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confidence: 99%

Spinal control of erection by glutamate in rats

Rampin¹,

Monnerie²,

Jerome³

et al. 2004

American Journal of Physiology-Regulatory, Integrative and Comp

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/ ajpregu.00645.2003.-The lumbosacral spinal network controlling penile erection is activated by information from peripheral and supraspinal origins. We tested the hypothesis that glutamate, released by sensory afferents from the genitals, activates this proerectile network. In anesthetized intact and T8 spinalized (i.e., freed from supraspinal inhibition) male rats, the parameters of electrical stimulation of the dorsal penile nerve (DPN) that elicited intracavernous pressure (ICP) rises were determined. In T8 spinalized rats, DPN stimulations were applied in the presence of D(Ϫ)-2-amino-5-phosphonopentanoic acid (D-AP5), a competitive NMDA receptor antagonist, or of 2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulphonamide (NBQX), an AMPA-kainate receptor antagonist, injected intrathecally at the lumbosacral level. Both antagonists, alone or in combination, dose dependently decreased the ICP rise and increased its latency. In conscious rats, reflexive erections were depressed by D-AP5 and NBQX, as revealed by an increased latency of the first erection and by decreases of the number of rats displaying erections, of the number of erection clusters and of the number of erections per cluster. In anesthetized rats, the combined administration of the glutamatergic agonists NMDA and AMPA elicited ICP rises in the absence of DPN stimulation. In contrast, both agonists moderately decreased the ICP rise elicited by DPN stimulation but did not affect its latency. These results support our hypothesis that glutamate, released on stimulation of the genitals and acting at AMPA and NMDA receptors, is a potent activator of the spinal proerectile network. urogenital; sexual reflexes; lumbosacral spinal cord ERECTION IS CAUSED by the simultaneous increase of blood flow to the penis and active relaxation of the erectile tissue of the corpora cavernosa and the corpus spongiosum (1). Both mechanisms are controlled by the autonomic nervous system.In conscious rats, retraction of the penile sheath elicits reflexive erections (14, 32) that are accompanied by penile pressure rises (5, 33). In anesthetized rats, intracavernous pressure (ICP) rises are reflexively elicited by stimulation of the dorsal penile nerve (DPN) (27,29,35). Reflexive erections rely on a reflex loop that includes a network of lumbosacral spinal neurons as a link between the DPN as the afferent limb and the sacral parasympathetic outflow as the efferent limb. The DPN conveys sensory information from the penis and perigenital skin to the lumbosacral cord (23, 26). Its stimulation activates a network of lumbosacral neurons (30). In rats, the proerectile parasympathetic outflow originates in the sacral parasympathetic nucleus (SPN) of the L6-S1 spinal cord (28). The SPN contains the preganglionic neurons that innervate the penis (21). The neurotransmitters that activate the spinal proerectile network are presently unknown.The role of glutamate in the spinal control of the urinary and the lower digestive tracts has been established. In the rat, the NMDA gl...

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“…Moreover, the activation of the group IV muscle afferents also modulates the motor drive to the skeletal (Ling et al, 2003) and respiratory muscles (Decherchi et al, 2007;Jammes et al, 1986) through their projections on spinal motor neurones and brain stem neurones. Glutamate is the most abundant and potent excitatory neurotransmitter in the mammalian central nervous system (Collingridge and Lester, 1989) and it is also an established transmitter of excitatory motor pathways in the spinal cord (Gougis et al, 2002), including the phrenic motoneurones (Issa et al, 2010;Mantilla et al, 2012). Because glutamate is suspected to modulate the HSP expression in several brain structures (Ayala and Tapia, 2003) and in culture of spinal cord slices (Guzmán-Lenis et al, 2008), it could be a possible candidate for the widespread HSP response to tibialis anterior (TA) stimulation.…”

Section: Research Articlementioning

confidence: 99%

“…Glutamate was also suspected to modulate the HSP70 expression in several brain structures (Ayala and Tapia, 2003) and the spinal cord (Guzmán-Lenis et al, 2008). The α1 adrenergic receptors have been identified in skeletal (Ives et al, 2012) and respiratory muscles (Aaker and Laughlin, 2002), kidney (Liu et al, 2011) and brain (Karczewski et al, 2012), and glutamate is the most abundant excitatory neurotransmitter in the central nervous system (Collingridge and Lester, 1989) and spinal cord (Gougis et al, 2002), including the phrenic motoneurones (Issa et al, 2010;Mantilla et al, 2012). The present study allows us to eliminate the possibility that glutamatergic neurotransmission is responsible for the widespread pHSP25 response to muscle fatigue.…”

Section: Pharmacological Approaches To Study the Efferent Arms Of Phsmentioning

confidence: 99%

The mechanisms of the widespread production of phosphorylated HSP25 after fatiguing muscle stimulation

Jammes

Steinberg

Olivier

et al. 2013

Journal of Experimental Biology

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Summary We already showed a widespread heat shock protein (HSP) response to fatigue of a single hindlimb muscle, responsible for a global adaptive response to an acute localized stress. We also demonstrated that the HSP response resulted from the activation of nerve afferents from the stimulated muscle. However, we did not examine the role played by the different muscle afferents as well as the efferent arm of HSP response. We here measured the changes in phosphorylated HSP25 (pHSP25) levels in resting hindlimb muscles, the diaphragm, kidney, and brain in response to a fatiguing stimulation of one tibialis anterior (TA) muscle which was repeated in five series of experiments: 1) intact muscle innervation, 2) during the selective procaine block of conduction in group IV muscle afferents, 3) after muscle nerve transection to suppress all the sensory messages, under pharmacological blockade of the 4) alpha adrenergic or 5) glutamatergic neurotransmission. The data showed that: 1) the pHSP25 response in hindlimb muscles resulted from the stimulation of both the groups III and IV muscle afferents while the pHSP25 response in the diaphragm, kidney, and brain resulted from the sole activation of the group IV fibres, 2) the blockade of alpha adrenergic, but not that of glutamatergic neurotransmission, suppressed the pHSP25 response in all the explored tissues except the brain. The present study highlights the role played by the groups III and IV muscle afferents in the fatigue-induced pHSP25 response and shows that the sympathetic nerve supply to the muscles and kidney represents the efferent arm of the pHSP25 activation. However, the pHSP25 changes in the brain cannot be explained by the pathways investigated here.

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Presence of the N-methyl-d-aspartic acid R1 glutamatergic receptor subunit in the lumbosacral spinal cord of male rats

Cited by 16 publications

References 18 publications

Anatomical evidence for glutamatergic transmission in primary sensory neurons and onto postganglionic neurons controlling penile erection in rats: an ultrastructural study with neuronal tracing and immunocytochemistry

Anatomical evidence for glutamatergic transmission in primary sensory neurons and onto postganglionic neurons controlling penile erection in rats: an ultrastructural study with neuronal tracing and immunocytochemistry

Spinal control of erection by glutamate in rats

The mechanisms of the widespread production of phosphorylated HSP25 after fatiguing muscle stimulation

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