Changes in serotonin level in the hypoglossal nucleus region during carbachol-induced atonia

Kubin, Leszek; Reignier, Clotilde; Tojima, Hirokazu; Taguchi, Osamu; Pack, Allan I.; Davies, Richard O.

doi:10.1016/0006-8993(94)91663-2

Cited by 90 publications

(48 citation statements)

References 45 publications

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“…Genioglossus muscle activity is under both serotonergic and noradrenergic state-dependent, especially sleep-wake, modulation (AstonJones and Bloom, 1981;Siegel, 1994;Kubin et al, 1998). The withdrawal of serotonergic (Jacobs and Azmitia, 1992;Kubin et al, 1994) and noradrenergic (Fenik et al, 2005) inputs depresses XII nerve activity during sleep or REM sleep-like states induced by pontine carbachol injections. Moreover, when serotonin is applied to the XII nucleus during sleep in behaving rats, genioglossus muscle activity increases (Jelev et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

Episodic Stimulation of α1-Adrenoreceptors Induces Protein Kinase C-Dependent Persistent Changes in Motoneuronal Excitability

Neverova¹,

Saywell²,

Nashold³

et al. 2007

J. Neurosci.

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In vitro long-term facilitation (ivLTF) is a novel form of activity-independent postsynaptic enhancement of AMPA receptor function in hypoglossal (XII) motoneurons that can be induced by intermittent activation of 5-HT 2 receptors. In vivo respiratory long-term facilitation (LTF) is characterized by a persistent 5-HT 2 receptor-dependent increase in respiratory motor output or ventilation after episodic exposures to hypoxia in adult rats. Here, we demonstrate that ivLTF can also be induced by episodic but not continuous stimulation of ␣1-adrenergic receptors that requires protein kinase C (PKC), but not PKA (protein kinase A), activation. Additionally, we show that in vivo respiratory LTF is also ␣1-adrenergic receptor dependent. We suggest that, in vivo, concurrent episodic activation of 5-HT 2 and ␣1-adrenergic receptors is necessary to produce long-lasting changes in the excitability of respiratory motoneurons, possibly involving PKC activation via the G␣ q -PLC (phospholipase C) signaling pathway common to both receptor subtypes. Such plasticity of XII motor output may increase upper airway muscle (innervated by XII nerve) tone and improve the likelihood that airway patency will be maintained. Elucidating the mechanism underlying LTF can be of clinical importance to the patients suffering from sleep-disordered breathing.

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Section: Discussionmentioning

confidence: 99%

Episodic Stimulation of α1-Adrenoreceptors Induces Protein Kinase C-Dependent Persistent Changes in Motoneuronal Excitability

Neverova¹,

Saywell²,

Nashold³

et al. 2007

J. Neurosci.

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“…Among cranial motoneurons, the mechanism of inhibition varies during REM sleep. For example, in trigeminal motoneurons (649-651, 965, 1029), inhibition is glycinergic, whereas the inhibition of hypoglossal motoneuron activity results primarily from disfacilitation (669,670,672,1378). The mechanisms underlying this differential control are incompletely understood but remain of considerable interest because of their potential involvement in conditions such as cataplexy, REM behavior disorder, and state-dependent respiratory disorders such as obstructive sleep apnea and perhaps sudden infant death syndrome.…”

Section: C) Presynaptic Actions Of Gaba a Receptorsmentioning

confidence: 99%

Synaptic Control of Motoneuronal Excitability

Rekling

Funk

Bayliss

et al. 2000

Physiological Reviews

537

482

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Movement, the fundamental component of behavior and the principal extrinsic action of the brain, is produced when skeletal muscles contract and relax in response to patterns of action potentials generated by motoneurons. The processes that determine the firing behavior of motoneurons are therefore important in understanding the transformation of neural activity to motor behavior. Here, we review recent studies on the control of motoneuronal excitability, focusing on synaptic and cellular properties. We first present a background description of motoneurons: their development, anatomical organization, and membrane properties, both passive and active. We then describe the general anatomical organization of synaptic input to motoneurons, followed by a description of the major transmitter systems that affect motoneuronal excitability, including ligands, receptor distribution, pre-and postsynaptic actions, signal transduction, and functional role. Glutamate is the main excitatory, and GABA and glycine are the main inhibitory transmitters acting through ionotropic receptors. These amino acids signal the principal motor commands from peripheral, spinal, and supraspinal structures. Amines, such as serotonin and norepinephrine, and neuropeptides, as well as the glutamate and GABA acting at metabotropic receptors, modulate motoneuronal excitability through pre-and postsynaptic actions. Acting principally via second messenger systems, their actions converge on common effectors, e.g., leak K + current, cationic inward current, hyperpolarization-activated inward current, Ca 2+ channels, or presynaptic release processes. Together, these numerous inputs mediate and modify incoming motor commands, ultimately generating the coordinated firing patterns that underlie muscle contractions during motor behavior.

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“…HMs receive a serotonergic innervation from caudal medullary raphe neurons (Manaker and Tischler, 1993), the activity of which is correlated with both sleep-wake states and rhythmic motor activities such as breathing (Jacobs and Azmitia, 1992;Jacobs and Fornal, 1993;Veasey et al, 1995;Fornal et al, 1996). Moreover, Kubin and colleagues have shown in vivo that 5-HT has excitatory effects on HMs (Kubin et al, 1992) and that diminished release of 5-HT and depression of hypoglossal activity are tightly coupled during experimentally induced REM-like sleep (Kubin et al, 1994). Thus, increased levels of 5-HT released during waking states (when raphe neurons are active) may confer an excitatory bias to HMs; the withdrawal of 5-HT during REM sleep states (when raphe neurons are silent) can lead to decreased HM excitability via disfacilitation, potentially contributing to the loss of tone in tongue muscles and obstructive apneas that occur during REM sleep (Remmers et al, 1978;Wiegand et al, 1991).…”

Section: Functional Consequencesmentioning

confidence: 99%

Postnatal Development of Serotonergic Innervation, 5-HT_1AReceptor Expression, and 5-HT Responses in Rat Motoneurons

1997

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We compared the electrophysiological responses to serotonin (5-HT) of neonatal and juvenile rat hypoglossal motoneurons (HMs) by using intracellular recording techniques in a brainstem slice preparation. In neonatal HMs (ՅP8), 5-HT caused a substantial decrease in the amplitude of spike afterhyperpolarization (AHP) that was associated with an increase in the minimal repetitive firing frequency (F min ). Previous work has shown that this effect of 5-HT was mediated by the 5-HT 1A receptor and may be secondary to inhibition of N-and P/Q-type calcium channels. In contrast to results from neonates, we found that 5-HT did not inhibit the AHP in juvenile HMs (Ն P20). Application of a cocktail of calcium channel toxins (-Conotoxin-GVIA and -Agatoxin-IVA) to juvenile HMs substantially inhibited the AHP, indicating that calcium entry through N-and P/Q-type channels supports the AHP in juvenile HMs, as it does in neonates. In addition, intracellular injection of the long-lasting GTP analog GTP␥S induced an agonist-independent increase in F min similar to that seen in neonates in the presence of 5-HT. Together, these results suggested that intracellular mechanisms downstream of the 5-HT 1A receptor capable of inhibiting the AHP were intact in juvenile HMs. Therefore, we investigated the possibility that age-related changes in effects of 5-HT on the AHP resulted from altered expression of the 5-HT 1A receptor. To this end, we performed ligand-binding autoradiography using [ 3 H]8-OH-DPAT, a 5-HT 1A agonist, and in situ hybridization using radiolabeled oligonucleotide probes specific for the 5-HT 1A receptor. The two approaches gave remarkably similar results. The highest levels of 5-HT 1A receptor expression were found in neonatal HMs, with maximal binding and hybridization at approximately postnatal day 7 (P7) and only low levels of receptor expression by P28. Finally, immunohistochemistry for 5-HT revealed that these developmental changes in 5-HT 1A receptor expression occurred coincident with a postnatal increase in serotonergic innervation of the hypoglossal nucleus (nXII). Together, these findings indicate that developmental changes occur in the serotonergic innervation of nXII and in the expression of 5-HT 1A receptors in HMs during the early postnatal period, resulting in markedly different effects of 5-HT on firing behavior in neonatal and juvenile HMs.

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Changes in serotonin level in the hypoglossal nucleus region during carbachol-induced atonia

Cited by 90 publications

References 45 publications

Episodic Stimulation of α1-Adrenoreceptors Induces Protein Kinase C-Dependent Persistent Changes in Motoneuronal Excitability

Episodic Stimulation of α1-Adrenoreceptors Induces Protein Kinase C-Dependent Persistent Changes in Motoneuronal Excitability

Synaptic Control of Motoneuronal Excitability

Postnatal Development of Serotonergic Innervation, 5-HT_1AReceptor Expression, and 5-HT Responses in Rat Motoneurons

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Changes in serotonin level in the hypoglossal nucleus region during carbachol-induced atonia

Cited by 90 publications

References 45 publications

Episodic Stimulation of α1-Adrenoreceptors Induces Protein Kinase C-Dependent Persistent Changes in Motoneuronal Excitability

Episodic Stimulation of α1-Adrenoreceptors Induces Protein Kinase C-Dependent Persistent Changes in Motoneuronal Excitability

Synaptic Control of Motoneuronal Excitability

Postnatal Development of Serotonergic Innervation, 5-HT1AReceptor Expression, and 5-HT Responses in Rat Motoneurons

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Product

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Postnatal Development of Serotonergic Innervation, 5-HT_1AReceptor Expression, and 5-HT Responses in Rat Motoneurons