Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats

Abstract

A total of 260 neurons were recorded in the rostral pontine tegmentum of freely moving cats during the sleep-waking cycle. Of these, 207 neurons (80%) were located in the dorsal pontine tegmentum containing monoaminergic and choline acetyltransferase (ChAT)-immunoreactive, or cholinergic neurons. In addition to presumably monoaminergic PS-off cells (n = 51) showing a cessation of discharge during paradoxical sleep (PS) and presumably cholinergic PGO-on cells (n = 40) exhibiting a burst of discharge just prior to and during ponto-geniculo-occipital (PGO) waves, we observed tonic (n = 108) and phasic (n = 61) neurons exhibiting, respectively, tonic and phasic patterns of discharge during wakefulness and/or paradoxical sleep. Of 87 tonic cells histologically localized in the dorsal pontine tegmentum rich in cholinergic neurons, 46 cells (53%) were identified as giving rise to ascending projections either to the intralaminar thalamic complex (n = 26) or to the ventrolateral posterior hypothalamus (n = 13) or to both (n = 9). Two types of tonic neurons were distinguished: 1) tonic type I neurons (n = 28), showing a tonic pattern and high rates of discharge during both waking and paradoxical sleep as compared with slow wave sleep; and 2) tonic type II neurons (n = 20), exhibiting a tonic pattern of discharge highly specific to the periods of paradoxical sleep. Tonic type I neurons were further divided into two subclasses on the basis of discharge rates during waking: a) rapid (Type I-R; n = 17); and b) slow (Type I-S; n = 11) units with a discharge frequency of more than 12 spikes/s or less than 5 spikes/s, respectively. Like monoaminergic PS-off and cholinergic PGO-on cells, both tonic type II and type I-S cells were characterized by a long spike duration (median: 3.3 and 3.5 ms), as well as by a slow conduction velocity (median = 1.8 and 1.7 m/s). In the light of these data, we discuss the possible cholinergic nature and functional significance of these ascending tonic neurons in the generation of neocortical electroencephalographic desynchronization occurring during waking and paradoxical sleep.

Noradrenaline hyperpolarizes identified rat mesopontine cholinergic neurons in vitro

“…Unfortunately, the behavioral neurophysiology of mesopontine cholinergic neurons is still not known with certainty. A small percentage of neurons in this region exhibit REM-selective discharge patterns, but the majority do not (El Mansari et al, 1989;. Based upon these data, have concluded that cholinergic neurons are active during both wake and REM sleep, while other authors have argued otherwise (Sakai, 1988;Kamondi et al, 1992).…”

Differential Effects of the Muscarinic M1 Receptor Agonist RS-86 and the Acetylcholine-Esterase Inhibitor Donepezil on REM Sleep Regulation in Healthy Volunteers

“…ACh release in the mPRF arises from the more rostral and dorsal cell groups comprising the laterodorsal (LDT) and the pedunculopontine tegmental (PPT) nuclei (Lydic and Baghdoyan, 1993). Consistently, LDT/PPT neurons demonstrate higher discharge rates during REM sleep (el Mansari et al, 1989). In humans, REM sleep is enhanced after administration of ACh-esterase inhibitors (Sitaram et al, 1976;Riemann et al, 1994) or cholinergic agonists (Spiegel, 1984;Riemann et al, 1988) and inhibited by anticholinergics (Sagales et al, 1969).…”

Noradrenergic Activation Amplifies Bottom-Up and Top-Down Signal-to-Noise Ratios in Sensory Thalamus

“…These dynamic changes are primarily caused by neuromodulators released in thalamus during specific behavioral states (Vanderwolf, 1988;Steriade and McCarley, 1990;Jones, 1993). In particular, cholinergic neurons in the LDT/PPT complex discharge vigorously during paradoxical sleep and also during wakefulness (el Mansari et al, 1989;, and the levels of acetylcholine increase in the thalamus during those states (Williams et al, 1994). Noradrenergic neurons in the LC discharge robustly during high levels of vigilance and attention, reduce their firing during slow-wave sleep, and stop firing during paradoxical sleep (Hobson et al, 1975;Foote et al, 1980;Aston-Jones and Bloom, 1981;Aston-Jones et al, 1991), and their firing produces forebrain activation (Berridge and Foote, 1991).…”