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The Journal of Neuroscience, April 2, 2008, 28(14):3535-3545; doi:10.1523/JNEUROSCI.5023-07.2008

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Behavioral/Systems/Cognitive
Glycinergic and GABA_A-Mediated Inhibition of Somatic Motoneurons Does Not Mediate Rapid Eye Movement Sleep Motor Atonia

Patricia L. Brooks¹ and John H. Peever^1,2

Departments of ¹Cell and Systems Biology and ²Physiology, Systems Neurobiology Laboratory, University of Toronto, Toronto, Ontario, Canada M5S 3G5

Correspondence should be addressed to Dr. John Peever, Department of Cell and Systems Biology, University of Toronto, 25 Harbord Street, Toronto, Ontario, Canada M5S 3G5. Email: John.Peever{at}utoronto.ca

A hallmark of rapid eye movement (REM) sleep is a potent suppression of postural muscle tone. Motor control in REM sleep is unique because it is characterized by flurries of intermittent muscle twitches that punctuate muscle atonia. Because somatic motoneurons are bombarded by strychnine-sensitive IPSPs during REM sleep, it is assumed that glycinergic inhibition underlies REM atonia. However, it has never been determined whether glycinergic inhibition of motoneurons is indeed responsible for triggering the loss of postural muscle tone during REM sleep. Therefore, we used reverse microdialysis, electrophysiology, and pharmacological and histological methods to determine whether glycinergic and/or GABA_A-mediated neurotransmission at the trigeminal motor pool mediates masseter muscle atonia during REM sleep in rats. By antagonizing glycine and GABA_A receptors on trigeminal motoneurons, we unmasked a tonic glycinergic/GABAergic drive at the trigeminal motor pool during waking and non-rapid eye movement (NREM) sleep. Blockade of this drive potently increased masseter muscle tone during both waking and NREM sleep. This glycinergic/GABAergic drive was immediately switched-off and converted into a phasic glycinergic drive during REM sleep. Blockade of this phasic drive potently provoked muscle twitch activity in REM sleep; however, it did not prevent or reverse REM atonia. Muscle atonia in REM even persisted when glycine and GABA_A receptors were simultaneously antagonized and trigeminal motoneurons were directly activated by glutamatergic excitation, indicating that a powerful, yet unidentified, inhibitory mechanism overrides motoneuron excitation during REM sleep. Our data refute the prevailing hypothesis that REM atonia is caused by glycinergic inhibition. The inhibitory mechanism mediating REM atonia therefore requires reevaluation.

Key words: sleep; REM; atonia; glycine; GABA; trigeminal; motoneuron; NREM sleep; REM sleep behavior disorder

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Received Nov. 12, 2007; revised Jan. 28, 2008; accepted Feb. 18, 2008.

Correspondence should be addressed to Dr. John Peever, Department of Cell and Systems Biology, University of Toronto, 25 Harbord Street, Toronto, Ontario, Canada M5S 3G5. Email: John.Peever{at}utoronto.ca

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