Noradrenergic neurotransmission in the brainstem is closely coupled to changes in muscle activity across the sleep‐wake cycle, and noradrenaline is considered to be a key excitatory neuromodulator that reinforces arousal‐related stimulus on motoneurons to drive movement. However, it is unknown if α‐1 noradrenoceptor activation increases motoneuron responsiveness to excitatory glutamate (AMPA) receptor‐mediated inputs during natural behaviour. Here, we studied the effects of noradrenaline on AMPA receptor‐mediated motor activity at the motoneuron level in freely‐behaving rats, particularly during rapid eye movement (REM) sleep, a period exhibiting both AMPA receptor‐triggered muscle twitches and periods of muscle quiescence during which AMPA drive is silent. Male rats were instrumented for electromyography and electroencephalography recording to monitor sleep and waking behaviour, while implantation of a cannula into the trigeminal motor nucleus of the brainstem allowed us to perfuse noradrenergic and glutamatergic drugs by reverse microdialysis, using masseter muscle activity as an index of motoneuronal output. We found that endogenous excitation of both α‐1 noradrenoceptor and AMPA receptors during waking are coupled to motor activity; however, REM sleep exhibits an absence of endogenous α‐1 noradrenoceptor activity. Importantly, exogenous α‐1 noradrenoceptor stimulation cannot reverse the muscle twitch suppression induced by AMPA receptor blockade, nor can it elevate muscle activity during quiet REM, a phase when endogenous AMPA receptor activity is subthreshold. We conclude that the presence of an endogenous glutamatergic drive is necessary for noradrenaline to trigger muscle activity at the level of the motoneuron in a naturally‐behaving animal. This article is protected by copyright. All rights reserved