ACTIVITY OF ROSTRAL TRIGEMINAL SENSORY NEURONS IN THE CAT DURING WAKEFULNESS AND SLEEP

1. Relatively little is known about the activity of trigeminal sensory neurons during naturally occurring behavioral states of sleep and wak efulness. Accordingly, experiments were performed in chronic unanesthe tized behaving cats in which neuronal activity in the rostral trigemin al sensory nuclear complex (TSNC) was recorded extracellularly in resp onse to low-intensity stimulation of mandibular and maxillary division s of cranial V nerve. The peripheral responses of TSNC neurons were ev aluated during naturally occurring episodes of wakefulness, quiet slee p, and active sleep. 2. The location of the rostral TSNC was confirmed by recording characteristic orthodromic field potentials generated in response to afferent volleys from tooth pulp and inferior alveolar (I AN) nerve stimuli. Antidromic fields from the trigeminal (MotV) and fa cial (MotVII) motor pools were used to demarcate the anterior and post erior limits of the rostral TSNC (i.e., main sensory nucleus and nucle us oralis pars,). 3. In the absence of peripherally applied stimuli, i ndividual rostral TSNC neurons recorded in the chronic, unanesthetized cat during the behavioral state of wakefulness did not display ongoin g spike activity. 4. The response characteristics of individual TSNC n eurons to low-intensity stimuli delivered to V afferents emanating fro m the canine tooth pulps during the behavioral state of drowsy wakeful ness consisted of a short train of action potentials characterized by a short latency-to-onset (7.2 +/- 0.4 ms, mean +/- SE, n = 51). TSNC n eurons fell into two categories on the basis of their response to grad ed intensities of tooth pulp stimuli. ''Stimulus intensity-dependent'' neurons demonstrated evoked responses that had a response profile tha t increased with stimulus intensity. In contrast, the response profile of ''stimulus intensity-independent'' neurons remained stable irrespe ctive of the stimulus intensity used. 5. During episodes of wakefulnes s and quiet sleep, IAN-evoked orthodromic fields did not differ in the ir amplitude or other waveform parameters. However, during active slee p, the IAN-evoked orthodromic field potential was suppressed by an ave rage of 28% as compared with wakefulness. 6. The number of action pote ntials evoked by consecutive presentation of low-intensity tooth pulp stimuli were compared during sleep and wakefulness. The evoked respons es were suppressed during active sleep (29%, n = 42). Suppression obse rved during active sleep occurred in both( ''stimulus-dependent'' and ''stimulus-independent'') groups of TSNC neurons. During the phasic ra pid-eye-movement (REM) episodes of active sleep, both the orthodromic held potentials and unitary action potentials were further suppressed or abolished. 7. The conclusion is reached that synaptic transmission through the rostral trigeminal sensory nucleus is dependent on the beh avioral state of the animal. We suggest that trigeminal sensory neuron s receiving input from canine pulpal afferents are subjected to a desc ending inhibitory drive that is engaged specifically during the behavi oral state of active sleep.