Active-sleep-related suppression of feline trigeminal sensory neurons: evidence implicating presynaptic inhibition via a process of primary afferent depolarization

Abstract

1. Changes in the excitability of lumbar and trigeminal primary afferent terminals have long been used as an index of primary afferent depolarization (PAD). PAD has been linked in part to the presynaptic inhibition of neurotransmission. During the behavioral state of active sleep, synaptic transmission through the rostral trigeminal sensory nuclear complex (TSNC) is suppressed when compared with other states such as wakefulness or quiet sleep. The mechanism underlying the suppression of neuronal activity in the rostral TSNC during active sleep is not known. Accordingly, experiments were conducted to determine, by examining the excitability of tooth pulp afferent terminals in cat during sleep and wakefulness, whether PAD processes might contribute in part to the suppression of rostral TSNC neuron activity. 2. Unitary potentials recorded in the maxillary canine tooth pulp were evoked by low-intensity stimuli applied to the rostral TSNC. Unitary potentials were identified by their "all-or-nothing" response, their invariant amplitude and latency, and their ability to follow a short train of high-frequency (333 Hz) stimuli. 3. The firing index (FI), a measure of the probability of evoking a unitary potential, was used to assess the changes in excitability of tooth pulp primary afferents. The proximity of stimulating electrodes to the terminal segment rather than a nonterminal segment of a tooth pulp afferent was demonstrated by observing an increase in the FI as a consequence of conditioning stimuli applied to ipsilateral branches of the trigeminal nerves. Increases in the FI over baseline were obtained for conditioning test intervals ranging from 20 to 80 ms, with the peak effect of conditioning occurring at 30 ms. 4. A total of 25 tooth pulp afferent terminals were identified and changes in their FI were examined during wakefulness, quiet sleep, and active sleep. The FI for all 25 terminals during wakefulness (FIW: 0.29 +/- 0.04, mean +/- SE) did not differ from that during quiet sleep (0.32 +/- 0.04). However, when compared with wakefulness, the FI during active sleep (FIAS: 0.52 +/- 0.07) was increased. The mean ratio of change in the FI (FIAS/FIW) was 3.5 +/- 0.9. These findings indicate that, as a population, tooth pulp afferent terminals are depolarized during the state of active sleep and that PAD processes may partly underlie the suppression of synaptic transmission through the rostral TSNC during this state. 5. To explore whether presynaptic excitability changes underlie the modulation of rostral TSNC neuron activity during active sleep, additional experiments were performed in which tooth-pulp-evoked responses of individual rostral TSNC neurons and the FIs of adjacent individual tooth pulp afferent terminals were analyzed as a function of sleep and wakefulness. The results indicated that active-sleep-related PAD was associated with active-sleep-related suppression of tooth-pulp-evoked activity of rostral TSNC neurons. 6. The conclusion is reached that PAD processes contribute to the mechanism whereby synaptic activity through the rostral TSNC is suppressed during the behavioral state of active sleep.