Respiratory activation of the genioglossus muscle involves both non-NMDA and NMDA glutamate receptors at the hypoglossal motor nucleus in vivo

Steenland, Hendrik W.; Liu, H.; Sood, Sandeep; Liu, X.; Horner, Richard L.

doi:10.1016/j.neuroscience.2005.12.040

Cited by 39 publications

(29 citation statements)

References 63 publications

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“…This drive is mainly glutamatergic (11,58), consistent with the evidence that many IRt XII premotor neurons use glutamate as their main transmitter (61). Other than that, little is known about the neurochemical features of IRt XII premotor neurons.…”

supporting

confidence: 61%

Hypoglossal premotor neurons of the intermediate medullary reticular region express cholinergic markers

Volgin¹,

Rukhadze²,

Kubin³

2008

Journal of Applied Physiology

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(IRt) region. This drive is mainly glutamatergic, but little is known about the neurochemical features of IRt XII premotor neurons. Prompted by the evidence that XII motoneuronal activity is controlled by both muscarinic (M) and nicotinic cholinergic inputs and that the IRt region contains cells that express choline acetyltransferase (ChAT), a marker of cholinergic neurons, we investigated whether some IRt XII premotor neurons are cholinergic. In seven rats, we applied single-cell reverse transcriptionpolymerase chain reaction to acutely dissociated IRt neurons retrogradely labeled from the XII nucleus. We found that over half (21/37) of such neurons expressed mRNA for ChAT and one-third (13/37) also had M2 receptor mRNA. In contrast, among the IRt neurons not retrogradely labeled, only 4 of 29 expressed ChAT mRNA (P Ͻ 0.0008) and only 3 of 29 expressed M2 receptor mRNA (P Ͻ 0.04). The distributions of other cholinergic receptor mRNAs (M1, M3, M4, M5, and nicotinic ␣4-subunit) did not differ between IRt XII premotor neurons and unlabeled IRt neurons. In an additional three rats with retrograde tracers injected into the XII nucleus and ChAT immunohistochemistry, 5-11% of IRt XII premotor neurons located at, and caudal to, the area postrema were ChAT positive, and 27-48% of ChAT-positive caudal IRt neurons were retrogradely labeled from the XII nucleus. Thus the pre-and postsynaptic cholinergic effects previously described in XII motoneurons may originate, at least in part, in medullary IRt neurons. inspiratory drive; muscarinic receptors; nicotinic receptors; single-cell reverse transcription-polymerase chain reaction; upper airway THE INSPIRATORY DRIVE TO HYPOGLOSSAL (XII) motoneurons originates in cells located between the ventrolateral border of the XII nucleus and nucleus ambiguus in the caudal medullary intermediate reticular (IRt) region (7,22,40,71). This drive is mainly glutamatergic (11, 58), consistent with the evidence that many IRt XII premotor neurons use glutamate as their main transmitter (61). Other than that, little is known about the neurochemical features of IRt XII premotor neurons.XII motoneurons innervate muscles of the tongue, including the genioglossus. In healthy individuals, the tongue has multiple functions related mainly to food intake and phonation. However, in obstructive sleep apnea (OSA) patients, the genioglossus and other upper airway muscles exhibit prominent tonic and phasic inspiratory activity, the function of which is to maintain the airway patent despite anatomic conditions that make the pharyngeal airway of these patients vulnerable to collapse (38, 60). Upper airway motor tone in OSA patients is high in wakefulness, decreases during slow-wave sleep, and nearly disappears during rapid eye movement (REM) sleep (16,21,39,48,53). The neurochemical mechanisms that determine the state-dependent changes in upper airway motor tone are the subject of intense basic and clinical research motivated by prospects of uncovering a pharmacological treatment for OSA and other sleep-relat...

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supporting

confidence: 61%

Hypoglossal premotor neurons of the intermediate medullary reticular region express cholinergic markers

Volgin¹,

Rukhadze²,

Kubin³

2008

Journal of Applied Physiology

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“…These concentrations are 10,000-fold higher than the low nanomolar plasma and effect site concentrations expected to be present after intravenous doses in humans or intraperitoneal clinical doses of fentanyl in rats (772), and are thus not likely to be of clinical relevance. The relevance of this rodent model for human upper airway physiology is further put into doubt, since isoflurane in this rodent preparation augmented respiratory-related genioglossus activity (575,648,653,654), which is clearly different from what has been observed in humans (158) and decerebrate dogs (70), where hypoglossal nerve activity as well as genioglossus activity are potently depressed by volatile anesthetics.…”

Section: Effects On Upper Airway Musclesmentioning

confidence: 70%

“…In contrast, recent data in freely behaving adult rats suggest that under in vivo conditions when tonic excitatory drive is much stronger than in vitro and when reflex inputs are intact, NMDA-receptor activation of the hypoglossal motor nucleus may be more important for both tonic and respiratory-related phasic GG muscle activity than non-NMDA (AMPA)-receptor activation (653). Both glutamate receptor subtypes seem to play a role in respiratory neurotransmission in urethane-and halothane-anesthetized rats (654). Similarly, experiments in decerebrate vagotomized dogs showed that both NMDA and non-NMDA glutamate receptors as well as serotonin (71) importantly contributed to the baseline respiratory activity of canine inspiratory HMNs during hypercapnic hyperoxia (68,789).…”

Section: Neurotransmission In Hypoglossal Motoneuronsmentioning

confidence: 92%

Effects of Anesthetics, Sedatives, and Opioids on Ventilatory Control

Stuth

Stucke

Zuperku

2012

Comprehensive Physiology

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This article provides a comprehensive, up to date summary of the effects of volatile, gaseous, and intravenous anesthetics and opioid agonists on ventilatory control. Emphasis is placed on data from human studies. Further mechanistic insights are provided by in vivo and in vitro data from other mammalian species. The focus is on the effects of clinically relevant agonist concentrations and studies using pharmacological, that is, supraclinical agonist concentrations are de-emphasized or excluded.

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“…2, E and F). Because a glutamatergic mechanism relays inspiratory drive onto respiratory motoneurons (Funk et al 1993;Steenland et al 2006Steenland et al , 2008Zuperku et al 2008), dopamine should presumably amplify this drive. However, since inspiratory activity remained unaffected, we conclude that dopamine primarily activates trigeminal motoneurons by a D 1 -like receptor mechanism.…”

Section: Dopamine Excites Motoneurons By a D 1 -Like Receptor Mechanismmentioning

confidence: 99%

Dopamine triggers skeletal muscle tone by activating D₁-like receptors on somatic motoneurons

Schwarz¹,

Peever

2011

Journal of Neurophysiology

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Schwarz PB, Peever JH. Dopamine triggers skeletal muscle tone by activating D 1 -like receptors on somatic motoneurons. J Neurophysiol 106: 1299 -1309, 2011. First published June 8, 2011 doi:10.1152/jn.00230.2011The dopamine system plays an integral role in motor physiology. Dopamine controls movement by modulation of higher-order motor centers (e.g., basal ganglia) but may also regulate movement by directly controlling motoneuron function. Even though dopamine cells synapse onto motoneurons, which themselves express dopamine receptors, it is unknown whether dopamine modulates skeletal muscle activity. Therefore, we aimed to determine whether changes in dopaminergic neurotransmission at a somatic motor pool affect motor outflow to skeletal muscles. We used microinjection, neuropharmacology, electrophysiology, and histology to determine whether manipulation of D 1 -and D 2 -like receptors on trigeminal motoneurons affects masseter and/or tensor palatini muscle tone in anesthetized rats. We found that apomorphine (a dopamine analog) activated trigeminal motoneurons and triggered a potent increase in both masseter and tensor palatini tone. This excitatory effect is mediated by D 1 -like receptors because specific D 1 -like receptor activation strengthened muscle tone and blockade of these receptors prevented dopamine-driven activation of motoneurons. Blockade of D 1 -like receptors alone had no detectable effect on basal masseter/tensor palatini tone, indicating the absence of a functional dopamine drive onto trigeminal motoneurons, at least during isoflurane anesthesia. Finally, we showed that D 2 -like receptors do not affect either trigeminal motoneuron function or masseter/tensor palatini muscle tone. Our results provide the first demonstration that dopamine can directly control movement by manipulating somatic motoneuron behavior and skeletal muscle tone.

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Respiratory activation of the genioglossus muscle involves both non-NMDA and NMDA glutamate receptors at the hypoglossal motor nucleus in vivo

Cited by 39 publications

References 63 publications

Hypoglossal premotor neurons of the intermediate medullary reticular region express cholinergic markers

Hypoglossal premotor neurons of the intermediate medullary reticular region express cholinergic markers

Effects of Anesthetics, Sedatives, and Opioids on Ventilatory Control

Dopamine triggers skeletal muscle tone by activating D₁-like receptors on somatic motoneurons

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Respiratory activation of the genioglossus muscle involves both non-NMDA and NMDA glutamate receptors at the hypoglossal motor nucleus in vivo

Cited by 39 publications

References 63 publications

Hypoglossal premotor neurons of the intermediate medullary reticular region express cholinergic markers

Hypoglossal premotor neurons of the intermediate medullary reticular region express cholinergic markers

Effects of Anesthetics, Sedatives, and Opioids on Ventilatory Control

Dopamine triggers skeletal muscle tone by activating D1-like receptors on somatic motoneurons

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Dopamine triggers skeletal muscle tone by activating D₁-like receptors on somatic motoneurons