Synaptic Mechanisms and Circuitry Involved in Motoneuron Control During Sleep

Abstract

Spontaneous amplitude fluctuations of the brainstem monosynaptic trigeminal jaw-closing reflex were examined in the freely moving chronic cat during wakefulness, quiet sleep, and active sleep. The largest amplitude responses occurred during active wakefulness; they decreased in size during quiet sleep. The lowest amplitude responses occurred during active sleep. A chronic cat preparation was developed in order to record intracellularly from identified trigeminal motoneurons for prolonged period of time throughout the states of sleep and wakefulness. The membrane potential of trigeminal motoneurons exhibited fluctuations that were correlated with changes in the animal's behavioral state. The fundamental pattern consisted of (a) slight hyperpolarization during quiet sleep, compared to arousal or alert wakefulness, (b) little if any hyperpolarization during quiet sleep compared to quiet wakefulness, and (c) dramatic hyperpolarization when active sleep was compared to quiet sleep. Sustained spike activity of trigeminal motoneurons, when present during wakefulness, decreased in frequency or tended to occur in bursts when the animal was in quiet sleep. During active sleep, activity ceased except for a few isolated spikes or short-duration bursts of action potentials. Based on an analysis of antidromically induced spike potentials and monosynaptically induced postsynaptic potentials, it was concluded that postsynaptic inhibition of trigeminal motoneurons during active sleep acts to suppress somatic reflex activity and produce muscular atonia. A companion study of the membrane potential of lumbar motoneurons in the chronic, unanesthetized, undrugged, normally respiring cat was performed during sleep and wakefulness. The antidromic field potential, antidromic and orthodromic spike, EPSP, membrane input resistance, and rheobasic current of lumbar motoneurons were studied during sleep and wakefulness. No change in motoneuron excitability occurred when quiet wakefulness was compared to quiet sleep. Postsynaptic inhibition resulted in decrease in excitability during active sleep. Further phasic decreases in excitability, also due to postsynaptic inhibition, occurred during active sleep in conjunction with clusters of rapid eye movements. The mesencephalon, pons, and medulla were explored in a conditioning-test paradigm in an attempt to find a site where electrical stimulation induced a pattern of somatomotor reflex and motoneuron membrane potential modulation comparable to that which occurs spontaneously during sleep and wakefulness. In unanesthetized, freely moving cats during wakefulness and quiet sleep, electrical stimulation within and in the vicinity of the nucleus pontis oralis produced facilitation of the masseteric reflex, whereas during active sleep the identical stimulus resulted in potent suppression of the reflex.(ABSTRACT TRUNCATED AT 400 WORDS)