Skip to main content Accessibility help
×
Hostname: page-component-76dd75c94c-68sx7 Total loading time: 0 Render date: 2024-04-30T09:36:19.165Z Has data issue: false hasContentIssue false

20 - REM sleep regulation by cholinergic neurons: highlights from 1999 to 2009

from Section IV - Neuroanatomy and neurochemistry

Published online by Cambridge University Press:  07 September 2011

Christopher J. Watson
Affiliation:
University of Michigan
Helen A. Baghdoyan
Affiliation:
University of Michigan
Ralph Lydic
Affiliation:
University of Michigan
Birendra N. Mallick
Affiliation:
Jawaharlal Nehru University
S. R. Pandi-Perumal
Affiliation:
Somnogen Canada Inc, Toronto
Robert W. McCarley
Affiliation:
Harvard University, Massachusetts
Adrian R. Morrison
Affiliation:
University of Pennsylvania
Get access

Summary

Summary

Rapid eye movement (REM) sleep is a behavioral state initiated and maintained by the interaction of multiple neurotransmitters, including acetylcholine. Numerous studies confirm that cholinergic transmission contributes to the regulation of REM sleep. Cholinergic signaling in the basal forebrain modulates the cortical activation that occurs during REM sleep. It is also well documented that cholinergic transmission in the pontine reticular formation plays a role in REM-sleep generation and maintenance. This chapter highlights evidence supporting that acetylcholine regulates REM sleep and focuses on the mechanisms that regulate cholinergic transmission within arousal-regulating brain regions. The chapter also considers how other arousal-regulating neurotransmitters, such as hypocretin, GABA, adenosine, and opioids modulate both cholinergic signaling and REM sleep. A greater understanding of how neurotransmitter interactions regulate REM sleep will further clarify the role of cholinergic transmission in REM-sleep generation. Employing new analytical techniques will facilitate understanding the effects of multiple neurotransmitter interactions on physiologically relevant time scales. Capillary electrophoresis and biosensors, which can quantify neurochemical changes on the order of seconds, will allow insights that could not be achieved with more conventional sampling techniques.

Type
Chapter
Information
Rapid Eye Movement Sleep
Regulation and Function
, pp. 194 - 205
Publisher: Cambridge University Press
Print publication year: 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baghdoyan, H. A. & Lydic, R. (1999) M2 muscarinic receptor subtype in the feline medial pontine reticular formation modulates the amount of rapid eye movement sleep. Sleep 22: –47.CrossRefGoogle ScholarPubMed
Bernard, R., Lydic, R. & Baghdoyan, H. A. (2006) Hypocretin (orexin) receptor subtypes differentially enhance acetylcholine release and activate G protein subtypes in rat pontine reticular formation. J Pharmacol Exp Ther 317: –71.Google ScholarPubMed
Brischoux, F., Mainville, L. & Jones, B. E. (2008) Muscarinic-2 and orexin-2 receptors on GABAergic and other neurons in the rat mesopontine tegmentum and their potential role in sleep-wake control. J Comp Neurol 510: –30.CrossRefGoogle Scholar
Bruno, J. P., Gash, C., Martin, B. . (2006) Second-by-second measurement of acetylcholine release in prefrontal cortex. Eur J Neurosci 24: –57.CrossRefGoogle ScholarPubMed
Coleman, C. G., Baghdoyan, H. A. & Lydic, R. (2006) Dialysis delivery of an adenosine A2A agonist into the pontine reticular formation of C57BL/6J mouse increases pontine acetylcholine release and sleep. J Neurochem 96:–9.CrossRefGoogle ScholarPubMed
Coleman, C. G., Lydic, R. & Baghdoyan, H. A. (2004) M2 muscarinic receptors in pontine reticular formation of C57BL/6J mouse contribute to rapid eye movement sleep generation. Neuroscience 126: –30.Google ScholarPubMed
Datta, S. & Maclean, R. R. (2007) Neurobiological mechanisms for the regulation of mammalian sleep-wake behavior: reinterpretation of historical evidence and inclusion of contemporary cellular and molecular evidence. Neurosci Biobehav Rev 31:–824.CrossRefGoogle ScholarPubMed
DeMarco, G. J., Baghdoyan, H. A. & Lydic, R. (2003) Differential cholinergic activation of G proteins in rat and mouse brainstem: relevance for sleep and nociception. J Comp Neurol 457: –84.CrossRefGoogle ScholarPubMed
DeMarco, G. J., Baghdoyan, H. A. & Lydic, R. (2004) Carbachol in the pontine reticular formation of C57BL/6J mouse decreases acetylcholine release in prefrontal cortex. Neuroscience 123: –29.CrossRefGoogle ScholarPubMed
Douglas, C. L., Baghdoyan, H. A. & Lydic, R. (2002) Postsynaptic muscarinic M1 receptors activate prefrontal cortical EEG of C57BL/6J mouse. J Neurophysiol 88: –9.CrossRefGoogle ScholarPubMed
Douglas, C. L., Bowman, G. N., Baghdoyan, H. A. . (2005) C57BL/6J and B6.V-LEPOB mice differ in the cholinergic modulation of sleep and breathing. J Appl Physiol 98: –29.CrossRefGoogle ScholarPubMed
Heister, D. S., Hayar, A. & Garcia-Rill, E. (2009) Cholinergic modulation of GABAergic and glutamatergic transmission in the dorsal subcoeruleus: mechanisms for REM sleep control. Sleep 32: –47.CrossRefGoogle ScholarPubMed
Hogg, R. C., Raggenbass, M. & Bertrand, D. (2003) Nicotinic acetylcholine receptors: from structure to function. Rev Physiol Biochem Pharmacol 147: –46.CrossRefGoogle Scholar
Ishii, M. & Kurachi, Y. (2006) Muscarinic acetylcholine receptors. Curr Pharm Des 12: –81.CrossRefGoogle ScholarPubMed
Jones, B. E. (2005) From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26:–CrossRefGoogle ScholarPubMed
Kanbayashi, T., Sugiyama, T., Aizawa, R. . (2002) Effects of donepezil (Aricept) on the rapid eye movement sleep of normal subjects. Psychiatry Clin Neurosci 56: –8.CrossRefGoogle ScholarPubMed
Kodama, T. & Honda, Y. (1999) Acetylcholine and glutamate release during sleep-wakefulness in the pedunculopontine tegmental nucleus and norepinephrine changes regulated by nitric oxide. Psychiatry Clin Neurosci 53: –11.CrossRefGoogle ScholarPubMed
Kubin, L. (2001) Carbachol models of REM sleep: recent developments and new directions. Arch Ital Biol 139: –68.Google ScholarPubMed
Lee, M. G., Hassani, O. K., Alonso, A. . (2005) Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci 25: –9.CrossRefGoogle ScholarPubMed
Lena, I., Parrot, S., Deschaux, O. . (2005) Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep–wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats. J Neurosci Res 81: –9.CrossRefGoogle ScholarPubMed
Lydic, R. & Baghdoyan, H. A. (2005) Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 103: –95.CrossRefGoogle ScholarPubMed
Lydic, R. & Baghdoyan, H. A. (2007) Neurochemical mechanisms mediating opioid-induced REM sleep disruption. In Sleep and Pain, eds. Lavigne, G., Sessle, B., Choinière, M. & Soja, P.. Seattle: IASP Press, pp. 99–122.Google Scholar
Lydic, R. & Baghdoyan, H. A. (2008) Acetylcholine modulates sleep and wakefulness: a synaptic perspective. In Neurochemistry of Sleep and Wakefulness, eds. Monti, J. M., Pandi-Perumal, S. R. & Sinton, C. M.. New York: Cambridge University Press, pp. 109–43.Google Scholar
Lydic, R., Douglas, C. L. & Baghdoyan, H. A. (2002) Microinjection of neostigmine into the pontine reticular formation of C57BL/6J mouse enhances rapid eye movement sleep and depresses breathing. Sleep 25: –41.CrossRefGoogle ScholarPubMed
Manfridi, A., Brambilla, D. & Mancia, M (2001) Sleep is differently modulated by basal forebrain GABA(A) and GABA(B) receptors. Am J Physiol Regul Integr Comp Physiol 281: –5.CrossRefGoogle ScholarPubMed
Marks, G. A., Sachs, O. W. & Birabil, C. G. (2008) Blockade of GABA, type A, receptors in the rat pontine reticular formation induces rapid eye movement sleep that is dependent upon the cholinergic system. Neuroscience 156:–10.CrossRefGoogle ScholarPubMed
Marks, G. A., Shaffery, J. P., Speciale, S. G. . (2003) Enhancement of rapid eye movement sleep in the rat by actions at A1 and A2a adenosine receptor subtypes with a differential sensitivity to atropine. Neuroscience 116: –20.CrossRefGoogle ScholarPubMed
McCarley, R. W. (2007) Neurobiology of REM and NREM sleep. Sleep Med 8: –30.CrossRefGoogle ScholarPubMed
McKenzie, J.A., Watson, C.J., Rostand, R.D. . (2002) Automated capillary liquid chromatography for simultaneous determination of neuroactive amines and amino acids. J Chromatogr A 962: –15.CrossRefGoogle ScholarPubMed
Nissen, C., Nofzinger, E.A., Feige, B. . (2006) Differential effects of the muscarinic M1 receptor agonist RS-86 and the acetylcholine-esterase inhibitor donepezil on REM sleep regulation in healthy volunteers. Neuropsychopharmacology 31:–300.CrossRefGoogle ScholarPubMed
Osman, N. I., Baghdoyan, H. A. & Lydic, R. (2005) Morphine inhibits acetylcholine release in rat prefrontal cortex when delivered systemically or by microdialysis to basal forebrain. Anesthesiology 103: –87.CrossRefGoogle ScholarPubMed
Porkka-Heiskanen, T., Alanko, L., Kalinchuk, A. . (2002) Adenosine and sleep. Sleep Med Rev 6: –32.CrossRefGoogle ScholarPubMed
Reinoso-Suarez, F., de Andrés, I., Rodrigo-Angulo, M. L. . (2001) Brain structures and mechanisms involved in the generation of REM sleep. Sleep Med Rev 5: –77.CrossRefGoogle ScholarPubMed
Salin-Pascual, R. J., Moro-Lopez, M. L., Gonzalez-Sanchez, H. . (1999) Changes in sleep after acute and repeated administration of nicotine in the rat. Psychopharmacology (Berl) 145: –8.CrossRefGoogle ScholarPubMed
Schredl, M., Hornung, O., Regen, F. . (2006) The effect of donepezil on sleep in elderly, healthy persons: a double-blind placebo-controlled study. Pharmacopsychiatry 39: –8.CrossRefGoogle ScholarPubMed
Smith, A., Watson, C. J., Frantz, K. J. . (2004) Differential increase in taurine levels by low-dose ethanol in the dorsal and ventral striatum revealed by microdialysis with on-line capillary electrophoresis. Alcohol Clin Exp Res 28: –38.CrossRefGoogle ScholarPubMed
Steriade, M. M. & McCarley, R. W. (2005) Brain Control of Wakefulness and Sleep. New York: Kluwer Academic/Plenum Publishers.Google Scholar
Tanase, D., Baghdoyan, H.A. & Lydic, R. (2003) Dialysis delivery of an adenosine A1 receptor agonist to the pontine reticular formation decreases acetylcholine release and increases anesthesia recovery time. Anesthesiology 98: –20.CrossRefGoogle ScholarPubMed
Van Dort, C. J., Baghdoyan, H. A. & Lydic, R. (2009) Adenosine A1 and A2A receptors in mouse prefrontal cortex modulate acetylcholine release and behavioral arousal. J Neurosci 29: –981.CrossRefGoogle Scholar
Vazquez, J. & Baghdoyan, H. A. (2001) Basal forebrain acetylcholine release during REM sleep is significantly greater than during waking. Am J Physiol Regul Integr Comp Physiol 280: –601.CrossRefGoogle ScholarPubMed
Vazquez, J. & Baghdoyan, H. A. (2003) Muscarinic and GABAA receptors modulate acetylcholine release in feline basal forebrain. Eur J Neurosci 17: –59.CrossRefGoogle ScholarPubMed
Vazquez, J. & Baghdoyan, H. A. (2004) GABAA receptors inhibit acetylcholine release in cat pontine reticular formation: implications for REM sleep regulation. J Neurophysiol 92: –206.CrossRefGoogle ScholarPubMed
Wagner, J. & Wagner, M. L. (2000) Non-benzodiazepines for the treatment of insomnia. Sleep Med Rev 4: –81.CrossRefGoogle ScholarPubMed
Watson, C. J., Lydic, R. & Baghdoyan, H. A. (2007) Sleep and GABA levels in the oral part of rat pontine reticular formation are decreased by local and systemic administration of morphine. Neuroscience 144: –86.CrossRefGoogle ScholarPubMed
Watson, C. J., Lydic, R. & Baghdoyan, H. A. (2008) Pontine reticular formation (PnO) administration of hypocretin-1 increases PnO GABA levels and wakefulness. Sleep 31: –64.CrossRefGoogle ScholarPubMed
Watson, C.J., Venton, B. J. & Kennedy, R. T. (2006) In vivo measurements of neurotransmitters by microdialysis sampling. Anal Chem 78: –9.CrossRefGoogle ScholarPubMed
Xi, M. C., Morales, F. R. & Chase, M. H. (2004) Interactions between GABAergic and cholinergic processes in the nucleus pontis oralis: neuronal mechanisms controlling active (rapid eye movement) sleep and wakefulness. J Neurosci 24: –8.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×