REM sleep-like atonia of hypoglossal (XII) motoneurons is caused by loss of noradrenergic and serotonergic inputs

American Journal of Respiratory and Critical Care Medicine

Volumn 172, Issue 10, 2005, Pages 1322-1330

  Fenik, Victor B ^a   Davies, Richard O ^a   Kubin, Leszek ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Hypoglossal motoneurons; Norepinephrine; Obstructive sleep apnea; Pons; Serotonin

Indexed keywords

CARBACHOL; METHYSERGIDE; PRAZOSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BREATHING RATE; CONTROLLED STUDY; DRUG EFFECT; DRUG WITHDRAWAL; ELECTROENCEPHALOGRAM; EXCITATION; HIPPOCAMPUS; HYPOGLOSSAL NERVE; MICROINJECTION; MOTONEURON; NERVE CONDUCTION; NONHUMAN; NORADRENERGIC NERVE; PRIORITY JOURNAL; RAT; REM SLEEP; SEROTONINERGIC NERVE CELL;

ADRENERGIC ANTAGONISTS; ANIMALS; CHOLINERGIC ANTAGONISTS; HYPOGLOSSAL NERVE; METHYSERGIDE; MOTOR NEURONS; NOREPINEPHRINE; PRAZOSIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROTRANSMITTER; RESPIRATORY MUSCLES; SEROTONIN; SLEEP, REM;

EID: 30444435074     PISSN: 1073449X     EISSN: 1073449X     Source Type: Journal    
DOI: 10.1164/rccm.200412-1750OC     Document Type: Article

References (56)

1. Remmers JE, DeGroot WJ, Sauerland EK, Anch AM. Pathogenesis of upper airway occlusion during sleep. J Appl Physiol 1978;44:931-938.
2. Kubin L, Davies RO, Pack AI. Control of upper airway motoneurons during REM sleep. News Physiol Sci 1998;13:91-97.
3. Kubin L, Davies RO. Mechanisms of airway hypotonia. In: Pack AI, editor. Sleep apnea: pathogenesis, diagnosis, and treatment. New York: Marcel Dekker; 2002. pp. 99-154.
4. Horner RL. The neuropharmacology of upper airway motor control in the awake and asleep states: implications for obstructive sleep apnoea. Respir Res 2001;2:286-294.
5. Malhotra A, White DP. Obstructive sleep apnoea. Lancet 2002;360:237-245.
6. Kubin L, Reignier C, Tojima H, Taguchi O, Pack AI, Davies RO. Changes in serotonin level in the hypoglossal nucleus region during the carbachol-induced atonia. Brain Res 1994;645:291-302.
7. Lai YY, Kodama T, Siegel J. Changes in monoamine release in the ventral horn and hypoglossal nucleus linked to pontine inhibition of muscle tone: an in vivo microdialysis study. J Neurosci 2001;21:7384-7391.
8. Chase MH, Morales F. The atonia and myoclonia of active (REM) sleep. Annu Rev Psychol 1990;41:557-584.
9. Mori S. Contribution of postural muscle tone to full expression of posture and locomotor movements: multi-faceted analyses of its setting brainstem-spinal cord mechanisms in the cat. Jpn J Physiol 1989;39:785-809.
10. Kubin L, Tojima H, Reignier C, Pack AI, Davies RO. Interaction of serotonergic excitatory drive to hypoglossal motoneurons with carbachol-induced, REM sleep-like atonia. Sleep 1996;19:187-195.
11. Jelev A, Sood S, Liu H, Nolan P, Horner RL. Microdialysis perfusion of 5-HT into hypoglossal motor nucleus differentially modulates genioglossus activity across natural sleep-wake states in rats. J Physiol 2001;532:467-481.
12. Kubin L, Kimura H, Tojima H, Davies RO, Pack AI. Suppression of hypoglossal motoneurons during the carbachol-induced atonia of REM sleep is not caused by fast synaptic inhibition. Brain Res 1993;611:300-312.
13. Morrison JL, Sood S, Liu H, Park E, Liu X, Nolan P, Horner RL. Role of inhibitory amino acids in control of hypoglossal motor outflow to genioglossus muscle in naturally sleeping rats. J Physiol 2003;552:975-991.
14. Fenik V, Davies RO, Kubin L. Combined antagonism of aminergic excitatory and amino acid inhibitory receptors in the XII nucleus abolishes REM sleep-like depression of hypoglossal motoneuronal activity. Arch Ital Biol 2004;142:237-249.
15. Kubin L. Carbachol models of REM sleep: recent developments and new directions. Arch Ital Biol 2001;139:147-168.
16. Fenik V, Marchenko V, Janssen P, Davies RO, Kubin L. A5 cells are silenced when REM sleep-like signs are elicited by pontine carbachol. J Appl Physiol 2002;93:1448-1456.
17. Fenik V, Davies RO, Kubin L. Noradrenergic, serotonergic and GABAergic antagonists injected together into the XII nucleus abolish the REM sleep-like depression of hypoglossal motoneuronal activity. J Sleep Res 2005;14 (In press)
18. Fenik V, Davies RO, Kubin L. Microinjections of serotonergic and noradrenergic antagonists into the XII nucleus abolish the carbachol-induced, REM sleep-like atonia of hypoglossal motoneurons. Program No. 769.9. 2003 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience; 2003. Available from: http://sfn.scholarone.com/itin2003/ (accessed September 2005).
19. Fenik V, Fenik P, Kubin L. A simple cuff electrode for nerve recording and stimulation in acute experiments on small animals. J Neurosci Methods 2001;116:147-150.
20. Nicholson C. Diffusion from an injected volume of a substance in the brain tissue with arbitrary volume fraction and tortuosity. Brain Res 1985;333:325-329.
21. Kubin L, Fenik V. Pontine cholinergic mechanisms and their impact on respiratory regulation. Respir Physiol Neurobiol 2004;143:235-249.
22. Paxinos G, Watson C. The rat brain in stereotaxic coordinates, 2nd ed. San Diego, CA: Academic Press; 1991.
23. Fenik V, Ogawa H, Davies RO, Kubin L. The activity of locus coeruleus neurons is reduced in urethane-anesthetized rats during carbachol-induced episodes of REM sleep-like suppression of upper airway motor tone. Soc Neurosci Abstr 1999;25:2144.
24. Baghdoyan HA. Cholinergic mechanisms regulating REM sleep. In: Schwartz WJ, editor. Sleep science: integrating basic research and clinical practice. Basel: Karger; 1997. pp. 88-116.
25. Vanni-Mercier G, Sakai K, Lin JS, Jouvet M. Mapping of cholinoceptive brainstem structures responsible for the generation of paradoxical sleep in the cat. Arch Ital Biol 1989;127:133-164.
26. Yamamoto K, Mamelak AN, Quattrochi JJ, Hobson JA. A cholinoceptive desynchronized sleep induction zone in the anterodorsal pontine tegmentum: locus of the sensitive region. Neuroscience 1990;39:279-293.
27. Kubin L, Tojima H, Davies RO, Pack AI. Serotonergic excitatory drive to hypoglossal motoneurons in the decerebrate cat. Neurosci Lett 1992;139:243-248.
28. 2- adrenergic receptors. FASEB J 1992;6:832-839.
29. Aston-Jones G, Shipley MT, Chouvet G, Ennis M, van Bockstaele E, Pieribone V, Shiekhattar R, Akaoka H, Drolet G, Astier B, et al. Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology. Prog Brain Res 1991;88:47-75.
30. Reiner PB. Correlational analysis of central noradrenergic neuronal activity and sympathetic tone in behaving cats. Brain Res 1986;378:86-96.
31. Al-Zubaidy ZA, Erickson RL, Greer JJ. Serotonergic and noradrenergic effects on respiratory neural discharge in the medullary slice preparation of neonatal rats. Pflugers Arch 1996;431:942-949.
32. Fenik V, Davies RO, Kubin L. Adrenergic receptor subtypes mediating excitatory effects in hypoglossal motoneurons. Sleep 1999;22:S37.
33. Veasey SC, Panckeri KA, Hoffman EA, Pack AI, Hendricks JC. The effects of serotonin antagonists in an animal model of sleep-disordered breathing. Am J Respir Crit Care Med 1996;153:776-786.
34. Veasey SC, Fenik P, Panckeri K, Pack AI, Hendricks JC. The effects of trazodone with L-trytophan on sleep-disordered breathing in the English bulldog. Am J Respir Crit Care Med 1999;160:1659-1667.
35. Fenik P, Veasey SC. Pharmacological characterization of serotonergic receptor activity in the hypoglossal nucleus. Am J Respir Crit Care Med 2003;167:563-569.
36. McGinty DJ, Harper RM. Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 1976;101:569-575.
37. Heym J, Steinfels GF, Jacobs BL. Activity of serotonin-containing neurons in the nucleus raphe pallidus of freely moving cats. Brain Res 1982;251:259-276.
38. Woch G, Davies RO, Pack AI, Kubin L. Behavior of raphe cells projecting to the dorsomedial medulla during carbachol-induced atonia in the cat. J Physiol 1996;490:745-758.
39. 1B receptors are the main postsynaptic mediators of adrenergic excitation in brainstem motoneurons: a single-cell RT-PCR study. J Chem Neuroanat 2001;22:157-166.
40. 2A receptor-like protein in the rat. J Comp Neurol 2000;418:323-345.
41. Zhan G, Shaheen F, Mackiewicz M, Fenik P, Veasey SC. Single cell laser dissection with molecular beacon polymerase chain reaction identifies 2A as the predominant serotonin receptor subtype in hypoglossal motoneurons. Neuroscience 2002;113:145-154.
42. Volgin DV, Fay R, Kubin L. Postnatal development of serotonin 1B, 2A and 2C receptors in brainstem motoneurons. Eur J Neurosci 2003;17:1179-1188.
43. Johansson O, Hokfelt T, Pernow B, Jeffcoate SL, White N, Steinbusch HW, Verhofstad AA, Emson PC, Spindel E. Immunohistochemical support for three putative transmitters in one neuron: coexistence of 5-hydroxytryptamine, substance P and thyrotropin releasing hormone-like immunoreactivity in medullary neurons projecting to the spinal cord. Neuroscience 1981;6:1857-1881.
44. Henry JN, Manaker S. Colocalization of substance P or enkephalin in serotonergic neuronal afferents to the hypoglossal nucleus in the rat. J Comp Neurol 1998;391:491-505.
45. Morales FR, Engelhardt JK, Soja PJ, Pereda AE, Chase MH. Motoneuron properties during motor inhibition produced by microinjection of carbachol into the pontine reticular formation of the decerebrate cat. J Neurophysiol 1987;57:1118-1129.
46. Yamuy J, Fung SJ, Xi M, Morales FR, Chase MH. Hypoglossal motoneurons are postsynaptically inhibited during carbachol-induced rapid eye movement sleep. Neuroscience 1999;94:11-15.
47. Fung SJ, Yamuy J, Xi MC, Engelhardt JK, Morales FR, Chase MH. Changes in electrophysiological properties of cat hypoglossal motoneurons during carbachol-induced motor inhibition. Brain Res 2000;885:262-272.
48. Kodama T, Lai YY, Siegel JM. Changes in inhibitory amino acid release linked to pontine-induced atonia: an in vivo microdialysis study. J Neurosci 2003;23:1548-1554.
49. Soja PJ, Finch DM, Chase MH. Effect of inhibitory amino acid antagonists on masseteric reflex suppression during active sleep. Exp Neurol 1987;96:178-193.
50. Aldes LD, Shaw B, Chronister RB, Haycock JW. Catecholamine-containing axon terminals in the hypoglossal nucleus of the rat: an immuno-electron microscopic study. Exp Brain Res 1990;81:167-178.
51. Altschuler SM, Bao X, Miselis RR. Dendritic architecture of hypoglossal motoneurons projecting to extrinsic tongue musculature in the rat. J Comp Neurol 1994;342:538-550.
52. Okabe S, Mackiewicz M, Kubin L. Serotonin receptor mRNA expression in the hypoglossal motor nucleus. Respir Physiol 1997;110:151-160.
53. Ursin R. Serotonin and sleep. Sleep Med Rev 2002;1:57-69.
54. Qureshi A, Lee-Chiong T Jr. Medications and their effects on sleep. Med Clin N Am 2004;88:751-766.
55. Veasey SC. Pharmacotherapies for obstructive sleep apnea: how close are we? Curr Opin Pulm Med 2001;7:399-403.
56. Smith IE, Quinnell TG. Pharmacotherapies for obstructive sleep apnoea: where are we now? Drugs 2004;64:1385-1399.