An Endogenous Glutamatergic Drive onto Somatic Motoneurons Contributes to the Stereotypical Pattern of Muscle Tone across the Sleep-Wake Cycle

Department of Cell and Systems Biology, Systems Neurobiology Laboratory, University of Toronto, Toronto, Ontario, Canada M5S 3G5.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 05/2008; 28(18):4649-60. DOI: 10.1523/JNEUROSCI.0334-08.2008
Source: PubMed


Skeletal muscle tone is modulated in a stereotypical pattern across the sleep-wake cycle. Abnormalities in this modulation contribute to most of the major sleep disorders; therefore, characterizing the neurochemical substrate responsible for transmitting a sleep-wake drive to somatic motoneurons needs to be determined. Glutamate is an excitatory neurotransmitter that modulates motoneuron excitability; however, its role in regulating motoneuron excitability and muscle tone during natural sleep-wake behaviors is unknown. Therefore, we used reverse-microdialysis, electrophysiology, pharmacological, and histological methods to determine how changes in glutamatergic neurotransmission within the trigeminal motor pool contribute to the sleep-wake pattern of masseter muscle tone in behaving rats. We found that blockade of non-NMDA and NMDA glutamate receptors (via CNQX and d-AP-5) on trigeminal motoneurons reduced waking masseter tone to sleeping levels, indicating that masseter tone is maximal during alert waking because motoneurons are activated by an endogenous glutamatergic drive. This wake-related drive is switched off in non-rapid eye movement (NREM) sleep, and this contributes to the suppression of muscle tone during this state. We also show that a functional glutamatergic drive generates the muscle twitches that characterize phasic rapid-eye movement (REM) sleep. However, loss of a waking glutamatergic drive is not sufficient for triggering the motor atonia that characterizes REM sleep because potent activation of either AMPA or NMDA receptors on trigeminal motoneurons was unable to reverse REM atonia. We conclude that an endogenous glutamatergic drive onto somatic motoneurons contributes to the stereotypical pattern of muscle tone during wakefulness, NREM sleep, and phasic REM sleep but not during tonic REM sleep.

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    Neuroscience Research 07/2015; 101. DOI:10.1016/j.neures.2015.07.004 · 1.94 Impact Factor
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    • "All electrophysiological signals were digitized at 200 Hz (AcqKnowledge software; Bio PAC, Goleta, CA, USA), monitored and stored on a computer. Two behavioral states were identified and classified according to the Christian Burgess's paper [11]. Alert wake (AW) was characterized by high levels of electrophysiological activity (i.e., chewing, grooming and drinking); quiet wake (QW) was characterized by the absence of overt motor activity. "
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    Physiology & Behavior 06/2014; 137. DOI:10.1016/j.physbeh.2014.06.017 · 2.98 Impact Factor
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    • "It has been shown in rats and cats that during REM sleep, in addition to a tonic GABA/glycinergic inhibition, the motoneurons receive phasic glutamate excitatory and Gly/GABA inhibitory inputs during the muscle twitches [16] [17] [56]. It has further been shown that the phasic glutamatergic inputs are responsible for the occurrence of muscle twitches, as the application of glutamate antagonists on motoneurons abolish them [17]. The localization of the neurons at the origin of these phasic glutamatergic inputs is not known. "
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