Activity of rostral trigeminal sensory neurons in the cat during wakefulness and sleep

Abstract

1. Relatively little is known about the activity of trigeminal sensory neurons during naturally occurring behavioral states of sleep and wakefulness. Accordingly, experiments were performed in chronic unanesthetized behaving cats in which neuronal activity in the rostral trigeminal sensory nuclear complex (TSNC) was recorded extracellularly in response to low-intensity stimulation of mandibular and maxillary divisions of cranial V nerve. The peripheral responses of TSNC neurons were evaluated during naturally occurring episodes of wakefulness, quiet sleep, 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 (IAN) nerve stimuli. Antidromic fields from the trigeminal (MotV) and facial (MotVII) motor pools were used to demarcate the anterior and posterior limits of the rostral TSNC (i.e., main sensory nucleus and nucleus oralis pars gamma). 3. In the absence of peripherally applied stimuli, individual rostral TSNC neurons recorded in the chronic, unanesthetized cat during the behavioral state of wakefulness did not display ongoing spike activity. 4. The response characteristics of individual TSNC neurons to low-intensity stimuli delivered to V afferents emanating from the canine tooth pulps during the behavioral state of drowsy wakefulness 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 neurons fell into two categories on the basis of their response to graded intensities of tooth pulp stimuli. "Stimulus intensity-dependent" neurons demonstrated evoked responses that had a response profile that increased with stimulus intensity. In contrast, the response profile of "stimulus intensity-independent" neurons remained stable irrespective of the stimulus intensity used. 5. During episodes of wakefulness and quiet sleep, IAN-evoked orthodromic fields did not differ in their amplitude or other waveform parameters. However, during active sleep, the IAN-evoked orthodromic field potential was suppressed by an average of 28% as compared with wakefulness. 6. The number of action potentials evoked by consecutive presentation of low-intensity tooth pulp stimuli were compared during sleep and wakefulness. The evoked responses were suppressed during active sleep (29%, n = 42). Suppression observed during active sleep occurred in both ("stimulus-dependent" and "stimulus-independent") groups of TSNC neurons. During the phasic rapid-eye-movement (REM) episodes of active sleep, both the orthodromic field 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 behavioral state of the animal.(ABSTRACT TRUNCATED AT 400 WORDS)