Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves

The only mesopontine neurons previously described as involved in the transfer of ponto-geniculo-occipital (PGO) waves from the brain stem to the thalamus were termed PGO-on bursting cells. We have studied, in chronically implanted cats, neuronal activities in brain-stem peribrachial (PB) and laterodorsal tegmental (LDT) cholinergic nuclei in relation to PGO waves recorded from the lateral geniculate (LG) thalamic nucleus during rapid-eye-movement (REM) sleep. We constructed peri-PGO histograms of PB/LDT cells' discharges and analyzed the interspike interval distribution during the period of increased neuronal activity related to PGO waves. Six categories of PGO-related PB/LDT neurons with identified thalamic projections were found: 4 classes of PGO-on cells: PGO-off but REM-on cells: and post-PGO cells. The physiological characteristics of a given cell class were stable even during prolonged recordings. One of these cell classes (1) represents the previously described PGO-on bursting neurons, while the other five (2–6) are newly discovered neuronal types. (1) Some neurons (16% of PGO-related cells) discharged stereotyped low-frequency (120– 180 Hz) spike bursts preceding the negative peak of the LG-PGO waves by 20–40 msec. These neurons had low firing rates (0.5–3.5 Hz) during all states. (2) A distinct cell class (22% of PGO-related neurons) fired high-frequency spike bursts (greater than 500 Hz) about 20–40 msec prior to the thalamic PGO wave. These bursts were preceded by a period (150–200 msec) of discharge acceleration on a background of tonically increased activity during REM sleep. (3) PGO-on tonic neurons (20% of PGO-related neurons) discharged trains of repetitive single spikes preceding the thalamic PGO waves by 100–150 msec, but never fired high- frequency spike bursts. (4) Other PGO-on neurons (10% of PGO-related neurons) discharged single spikes preceding thalamic PGO waves by 15–30 msec. On the basis of parallel intracellular recordings in acutely prepared, reserpine-treated animals, we concluded that the PGO-on single spikes arise from conventional excitatory postsynaptic potentials and do not reflect tiny postinhibitory rebounds. (5) A peculiar cellular class, termed PGO-off elements (8% of PGO-related neurons), consisted of neurons with tonic, high discharge rates (greater than 30 Hz) during REM sleep. These neurons stopped firing 100– 200 msec before and during the thalamic PGO waves. (6) Finally, other neurons discharged spike bursts or tonic spike trains 100–300 msec after the initially negative peak of the thalamic PGO field potential (post-PGO elements, 23% of PGO-related neurons).(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  M. Celio,et al.  Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. , 1986, Science.

[2]  Y. Frégnac,et al.  Lesion of the PGO pathways in the kitten. II. Impairment of physiological and morphological maturation of the lateral geniculate nucleus , 1989, Brain Research.

[3]  J. Hobson,et al.  REM sleep burst neurons, PGO waves, and eye movement information. , 1983, Journal of neurophysiology.

[4]  R. North,et al.  Agonists at μ‐opioid, M2 ‐muscarinic and GABAB ‐receptors increase the same potassium conductance in rat lateral parabrachial neurones , 1988, British journal of pharmacology.

[5]  M. Descheˆnes,et al.  The cellular mechanism of thalamic ponto-geniculo-occipital waves , 1989, Neuroscience.

[6]  R. McCarley,et al.  Intracellular evidence linking medial pontine reticular formation neurons to PGO wave generation , 1983, Brain Research.

[7]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. , 1983, Journal of neurophysiology.

[8]  M. Deschenes,et al.  Phasic activation of lateral geniculate and perigeniculate thalamic neurons during sleep with ponto-geniculo-occipital waves , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Professor Dr. John C. Eccles,et al.  The Cerebellum as a Neuronal Machine , 1967, Springer Berlin Heidelberg.

[10]  M. Jouvet,et al.  Brain stem PGO-on cells projecting directly to the cat dorsal lateral geniculate nucleus , 1980, Brain Research.

[11]  M. Steriade,et al.  Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  D. McCormick,et al.  Actions of acetylcholine in the guinea‐pig and cat medial and lateral geniculate nuclei, in vitro. , 1987, The Journal of physiology.

[13]  R. North,et al.  Acetylcholine hyperpolarizes central neurones by acting on an M2 muscarinic receptor , 1986, Nature.

[14]  J. Hobson,et al.  Ponto-geniculo-occipital (PGO) burst neurons: correlative evidence for neuronal generators of PGO waves. , 1978, Science.

[15]  I. Donaldson Control of gaze by brain stem neurons Proceedings of the symposium held in the Abbaye de Royaumont. Paris 12–15 July, 1977.Developments in Neuroscience, vol. 1.R. Baker &A. Berthoz (eds). Elsevier/North Holland Biomedical Press, Amsterdam (1977). 514 + xv pp., $59.95 , 1978, Neuroscience.

[16]  D. Prince,et al.  Printed in Great Britain , 2005 .

[17]  Barbara E. Jones,et al.  Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat. II. Effects upon sleep-waking states , 1988, Brain Research.

[18]  M. Jouvet,et al.  Discharge patterns of the nucleus parabrachialis lateralis neurons of the cat during sleep and waking , 1977, Brain Research.

[19]  H. Fibiger,et al.  Basal forebrain and mesopontine tegmental projections to the reticular thalamic nucleus: an axonal collateralization and immunohistochemical study in the rat , 1989, Brain Research.

[20]  M. Jouvet,et al.  Locus coeruleus et sommeil paradoxal , 1965 .

[21]  J. Deniau,et al.  Substantia nigra efferent connections. , 1979, Applied neurophysiology.

[22]  R. M. Bowker,et al.  The startle reflex and PGO spikes , 1976, Brain Research.

[23]  A. Proia,et al.  The reciprocal electrophysiological influence between the nucleus tegmenti pedunculopontinus and the substantia nigra in normal and decorticated rats , 1987, Brain Research.

[24]  M. Steriade,et al.  Brainstem Control of Wakefulness and Sleep , 1990, Springer US.

[25]  R. M. Beckstead,et al.  The distribution and some morphological features of substantia nigra neurons that project to the thalamus, superior colliculus and pedunculopontine nucleus in the monkey , 1982, Neuroscience.

[26]  C. Heizmann,et al.  Calcium-binding protein parvalbumin as a neuronal marker , 1981, Nature.

[27]  M. Jouvet,et al.  Effects of ponto-mesencephalic lesions and electrical stimulation upon PGO waves and EMPs in unanesthetized cats. , 1976, Electroencephalography and clinical neurophysiology.

[28]  S. T. Kitai,et al.  Electrophysiological properties of pedunculopontine neurons and their postsynaptic responses following stimulation of substantia nigra reticulata , 1990, Brain Research.

[29]  K. Wilcox,et al.  In vitro electrophysiology of neurons in the lateral dorsal tegmental nucleus , 1989, Brain Research Bulletin.

[30]  I S Curthoys,et al.  Anatomy of physiologically identified eye‐movement‐related pause neurons in the cat: Pontomedullary region , 1987, The Journal of comparative neurology.

[31]  G Oakson,et al.  Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  M. Steriade,et al.  Immediate behavioral effects of kainic acid injections into the midbrain reticular core , 1981, Behavioural Brain Research.

[33]  M. Jalfre,et al.  Drugs and PGO waves in the lateral geniculate body of the curarized cat. IV. The effects of acetylcholine, GABA and benzodiazepines on PGO wave activity. , 1976, Archives internationales de pharmacodynamie et de therapie.

[34]  M. Descheˆnes,et al.  The blockage of ponto-geniculo-occipital waves in the cat lateral geniculate nucleus by nicotinic antagonists , 1988, Brain Research.

[35]  R. M. Beckstead Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes , 1983, Neuroscience.

[36]  U. Gerber,et al.  Repetitive firing properties of medial pontine reticular formation neurones of the rat recorded in vitro. , 1989, The Journal of physiology.

[37]  R. Llinás,et al.  The functional states of the thalamus and the associated neuronal interplay. , 1988, Physiological reviews.

[38]  A. Morrison,et al.  The effects of tones on PGO waves in slow wave sleep and paradoxical sleep , 1989, Experimental Neurology.

[39]  H. Roffwarg,et al.  Ontogenetic development of the human sleep-dream cycle. , 1966, Science.