Enhanced Glutamate Release During REM Sleep in the Rostromedial Medulla As Measured by in Vivo Microdialysis

Overview

Journal Brain Res

Specialty Neurology

Date 1998 Mar 13

PMID 9497097

Citations 22

Authors

T Kodama

Y Y Lai

J M Siegel

Affiliations

Soon will be listed here.

Abstract

Anatomical studies and stimulation studies in the decerebrate animal have suggested that the muscle atonia of rapid eye movement (REM) sleep is mediated by a projection from cholinoceptive glutamatergic neurons in the pons to the nucleus magnocellularis (NMC) of medulla. This model suggests that glutamate release in NMC should be enhanced in REM sleep. In the present study, glutamate release across the sleep-wake cycle in NMC was measured by in vivo microdialysis. We found that glutamate release in NMC was significantly higher (p = 0.0252) during REM sleep than during wakefulness (W). Glutamate release during REM sleep was not elevated either in nucleus paramedianus (NPM) or in the pontine inhibitory area (PIA) regions where cholinergic stimulation suppresses muscle tone. Acetylcholine (ACh) microinjection into PIA enhanced glutamate release in NMC. These results support the hypothesis that a glutamatergic pathway from PIA to NMC is responsible for the suppression of muscle tone in REM sleep.

Citing Articles

The Metabotropic Glutamate 5 Receptor in Sleep and Wakefulness: Focus on the Cortico-Thalamo-Cortical Oscillations.

Ngomba R, Luttjohann A, Dexter A, Ray S, van Luijtelaar G Cells. 2023; 12(13).

PMID: 37443795 PMC: 10341329. DOI: 10.3390/cells12131761.

Sleep and Microdialysis: An Experiment and a Systematic Review of Histamine and Several Amino Acids.

Leenaars C, Drinkenburg W, Nolten C, Dematteis M, Joosten R, Feenstra M J Circadian Rhythms. 2019; 17:7.

PMID: 31303885 PMC: 6611484. DOI: 10.5334/jcr.183.

mGlu2 Receptor Agonism, but Not Positive Allosteric Modulation, Elicits Rapid Tolerance towards Their Primary Efficacy on Sleep Measures in Rats.

Ahnaou A, Lavreysen H, Tresadern G, Cid J, Drinkenburg W PLoS One. 2015; 10(12):e0144017.

PMID: 26658273 PMC: 4684355. DOI: 10.1371/journal.pone.0144017.

Deletion of Metabotropic Glutamate Receptors 2 and 3 (mGlu2 & mGlu3) in Mice Disrupts Sleep and Wheel-Running Activity, and Increases the Sensitivity of the Circadian System to Light.

Pritchett D, Jagannath A, Brown L, Tam S, Hasan S, Gatti S PLoS One. 2015; 10(5):e0125523.

PMID: 25950516 PMC: 4423919. DOI: 10.1371/journal.pone.0125523.

Pharmacological and pharmacokinetic properties of JNJ-40411813, a positive allosteric modulator of the mGlu2 receptor.

Lavreysen H, Ahnaou A, Drinkenburg W, Langlois X, Mackie C, Pype S Pharmacol Res Perspect. 2015; 3(1):e00096.

PMID: 25692015 PMC: 4317228. DOI: 10.1002/prp2.96.

References

Onoe H, Sakai K . Kainate receptors: a novel mechanism in paradoxical (REM) sleep generation. Neuroreport. 1995; 6(2):353-6. View

Bernath S . Calcium-independent release of amino acid neurotransmitters: fact or artifact?. Prog Neurobiol. 1992; 38(1):57-91. DOI: 10.1016/0301-0082(92)90035-d. View

Lai Y, Siegel J . Cardiovascular and muscle tone changes produced by microinjection of cholinergic and glutamatergic agonists in dorsolateral pons and medial medulla. Brain Res. 1990; 514(1):27-36. PMC: 9105767. DOI: 10.1016/0006-8993(90)90432-b. View

Henley K, Morrison A . A re-evaluation of the effects of lesions of the pontine tegmentum and locus coeruleus on phenomena of paradoxical sleep in the cat. Acta Neurobiol Exp (Wars). 1974; 34(2):215-32. View

George R, HASLETT W, JENDEN D . A CHOLINERGIC MECHANISM IN THE BRAINSTEM RETICULAR FORMATION: INDUCTION OF PARADOXICAL SLEEP. Int J Neuropharmacol. 1964; 3:541-52. DOI: 10.1016/0028-3908(64)90076-0. View

Magoun H . BULBAR INHIBITION AND FACILITATION OF MOTOR ACTIVITY. Science. 1944; 100(2607):549-50. DOI: 10.1126/science.100.2607.549. View

Lai Y, Clements J, Siegel J . Glutamatergic and cholinergic projections to the pontine inhibitory area identified with horseradish peroxidase retrograde transport and immunohistochemistry. J Comp Neurol. 1993; 336(3):321-30. PMC: 9046457. DOI: 10.1002/cne.903360302. View

Kodama T, Takahashi Y, Honda Y . Enhancement of acetylcholine release during paradoxical sleep in the dorsal tegmental field of the cat brain stem. Neurosci Lett. 1990; 114(3):277-82. DOI: 10.1016/0304-3940(90)90576-u. View

Holmes C, Jones B . Importance of cholinergic, GABAergic, serotonergic and other neurons in the medial medullary reticular formation for sleep-wake states studied by cytotoxic lesions in the cat. Neuroscience. 1994; 62(4):1179-200. DOI: 10.1016/0306-4522(94)90352-2. View

10.

Baghdoyan H, Rodrigo-Angulo M, McCarley R, Hobson J . Site-specific enhancement and suppression of desynchronized sleep signs following cholinergic stimulation of three brainstem regions. Brain Res. 1984; 306(1-2):39-52. DOI: 10.1016/0006-8993(84)90354-8. View

11.

Katayama Y, DeWitt D, Becker D, Hayes R . Behavioral evidence for a cholinoceptive pontine inhibitory area: descending control of spinal motor output and sensory input. Brain Res. 1984; 296(2):241-62. DOI: 10.1016/0006-8993(84)90062-3. View

12.

Lai Y, Siegel J . Corticotropin-releasing factor mediated muscle atonia in pons and medulla. Brain Res. 1992; 575(1):63-8. PMC: 9046436. DOI: 10.1016/0006-8993(92)90423-7. View

13.

Lai Y, Siegel J . Muscle tone suppression and stepping produced by stimulation of midbrain and rostral pontine reticular formation. J Neurosci. 1990; 10(8):2727-34. PMC: 6570267. View

14.

Westerink B, Damsma G, Rollema H, DE VRIES J, Horn A . Scope and limitations of in vivo brain dialysis: a comparison of its application to various neurotransmitter systems. Life Sci. 1987; 41(15):1763-76. DOI: 10.1016/0024-3205(87)90695-3. View

15.

Shiromani P, Siegel J, Tomaszewski K, McGinty D . Alterations in blood pressure and REM sleep after pontine carbachol microinfusion. Exp Neurol. 1986; 91(2):285-92. PMC: 9045734. DOI: 10.1016/0014-4886(86)90069-5. View

16.

Lai Y, Siegel J . Medullary regions mediating atonia. J Neurosci. 1988; 8(12):4790-6. PMC: 6569564. View

17.

Shiromani P, Lai Y, Siegel J . Descending projections from the dorsolateral pontine tegmentum to the paramedian reticular nucleus of the caudal medulla in the cat. Brain Res. 1990; 517(1-2):224-8. PMC: 9109500. DOI: 10.1016/0006-8993(90)91030-k. View

18.

Kodama T, Lai Y, Siegel J . Enhancement of acetylcholine release during REM sleep in the caudomedial medulla as measured by in vivo microdialysis. Brain Res. 1992; 580(1-2):348-50. PMC: 9046437. DOI: 10.1016/0006-8993(92)90967-e. View

19.

Mitler M, Dement W . Cataplectic-like behavior in cats after micro-injections of carbachol in pontine reticular formation. Brain Res. 1974; 68(2):335-43. PMC: 2475546. DOI: 10.1016/0006-8993(74)90402-8. View

20.

Lai Y, Siegel J, Wilson W . Effect of blood pressure on medial medulla-induced muscle atonia. Am J Physiol. 1987; 252(6 Pt 2):H1249-57. PMC: 9046434. DOI: 10.1152/ajpheart.1987.252.6.H1249. View