Presumed serotonin-containing neurons in the nucleus centralis superior (NCS) in freely moving cats showed a slow, rhythmic discharge rate during quiet waking (X = 2.41 +/- 0.12 spikes/s), and displayed a strong positive correlation with level of behavioral arousal. Unit activity during phasic and tonic arousal, as elicited by acoustic stimuli, was increased by 76% and 31%, respectively, and unit activity decreased to active waking levels as the arousal response habituated. During active waking, unit activity was significantly increased by 18% as compared to quiet waking, but there was no correlation between unit activity and phasic body movements. NCS unit activity showed a significant decrease of 15% during drowsiness (first appearance of EEG synchronization) as compared to quiet waking, and then progressive decreases during the early (-27%), middle (-41%) and late (-67%) phases of slow wave sleep. During all phases of slow wave sleep, the occurrence of sleep spindles was frequently associated with a transitory decrease in unit activity. The discharge rate would typically decrease during the few seconds immediately preceding the spindle, remain at this low level during the occurrence of the spindle, and then increase immediately after the spindle. NCS unit activity showed decreases of 73% during Pre-REM (the 60 s immediately before REM onset) and 84% during REM, as compared to quiet waking. Unit activity reappeared on the average 2.7 s before the end of REM with significant increases in activity of 60% and 28% during the first second and first 10 s of unit activity, respectively, as compared to quiet waking. NCS neurons showed no significant changes in activity across the 24-h light-dark cycle, when behavioral state was held constant. Seventy-eight % of NCS units were excited by phasic auditory stimulation, with a mean latency of 41 +/- 3 ms and a mean duration of 34 +/- 4 ms. The response to repetitive auditory stimulation showed no evidence of habituation and was even present during sleep. A similar response was evoked by phasic visual stimulation in 68% of the cells tested. A small subset of cells (12%) were inhibited by phasic auditory and visual stimuli. NCS neurons were inhibited by low doses of 5-methoxy-N,N-dimethyltryptamine (50 micrograms/kg, i.m.) or LSD (50 micrograms/kg, i.p.). These data demonstrate that serotonin-containing NCS neurons exhibit properties very similar to those in the nucleus raphe dorsalis, but are different in many respects from medullary serotonergic neurons.