Experimental Brain Research

, Volume 81, Issue 3, pp 533–544 | Cite as

Brainstem genesis of reserpine-induced ponto-geniculo-occipital waves: An electrophysiological and morphological investigation

  • D. Paré
  • R. Curró Dossi
  • S. Datta
  • M. Steriade


Several experimental results indicate that the peribrachial (PB) cholinergic area of the pedunculopontine nucleus is the final relay for the transfer of brainstem-generated pontogeniculo-occipital (PGO) waves to the thalamus. However, the mechanisms underlying the PGO-related activity of PB neurons remain unknown. In order to study these mechanisms, single unit recordings in the PB area were performed in reserpinized cats. Because PGO waves are closely related to rapid eye movements, our microelectrode explorations were also aimed to some structures of the preoculomotor network, namely, the superior colliculus (SC) and parts of the central tegmental field (FTC). We have found several classes of PGO-on cells in the PB area, most of them descharging 80 ms or less before the peak of PGO waves. These cell-classes comprised high-frequency bursting cells, slow-frequency bursting cells, and neurons discharging single spikes or doublets. Intracellular recordings showed that PGO-on single spikes arise from conventional excitatory postsynaptic potentials. Among PGO-related cells in structures outside the PB limits, it was found that most SC cells discharge during or after the PGO, whereas FTC cells increase their discharge rate several hundreds of ms before PGO waves, thus indicating that PGO waves are elaborated long before the activition of PB neurons. Massive retrograde labeling was found in FTC following horseradish peroxidase injections into the PB area. We suggest that long-lead FTC neurons provide an excitatory input to PGO-on PB neurons.

Key words

Ponto-geniculo-occipital (PGO) waves Peribrachial area Central tegmental field Superior colliculus Cat 


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  1. Beckstead RM (1983) Long collateral branches of substantia nigra pars reticulata axons to the thalamus, superior colliculus and reticular formation in monkey and cat: multiple retrograde neuronal labeling with fluorescent dyes. Neuroscience 10:767–779PubMedCrossRefGoogle Scholar
  2. Bon L, Corazza R, Inchingolo P (1980) Eye movements during the waking sleep cycle of the encéphale isolé semichronic cat preparation. Electroenceph Clin Neurophysiol 48:327–340PubMedCrossRefGoogle Scholar
  3. Brooks DC, Gershon MD (1971) Eye movement potentials in the oculomotor and visual systems of the cat: a comparison of reserpine induced waves with those present during wakefulness and rapid eye movement sleep. Brain Res 27:223–239PubMedCrossRefGoogle Scholar
  4. De Lima AD, Singer W (1987) The brainstem projection to the lateral geniculate nucleus in the cat: identification of cholinergic and monoaminergic elements. J Comp Neurol 259:92–121PubMedCrossRefGoogle Scholar
  5. Dement W, Kleitman N (1957) Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. Electroencephalogr Clin Neurol 9:673–690CrossRefGoogle Scholar
  6. Fuchs AF, Kaneko CRS, Scudder CA (1985) Brainstem control of saccadic eye movements. Ann Rev Neurosci 8:307–337PubMedCrossRefGoogle Scholar
  7. Fuchs AF, Ron S (1968) An analysis or rapid eye movements of sleep in the monkey. Electroenceph Clin Neurophysiol 25:244–251PubMedCrossRefGoogle Scholar
  8. Hallenger AE, Levey AI, Lee HJ, Rye DB, Wainer BH (1987) The origin of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262:105–124CrossRefGoogle Scholar
  9. Herman JH, Barker DR, Roffwarg HP (1983) Similarity of eye movement characteristics in REM sleep and the awake state. Psychophysiology 20:537–543PubMedGoogle Scholar
  10. Hobson JA, Steriade M (1986) Neuronal basis of behavioral state control. In: Mountcastle VB, Bloom FE (eds) Handbook of physiology, Sect 1, Vol IV. Am Physiol Soc, Bethesda, pp 701–823Google Scholar
  11. Hu B, Bouhassira D, Steriade M, Deschênes M (1988) The blockage of ponto-geniculo-occipital waves in the cat lateral geniculate nucleus by nicotinic antagonists. Brain Res 473:394–397PubMedCrossRefGoogle Scholar
  12. Hu B, Steriade M, Deschênes M (1989) The cellular mechanisms of thalamic ponto-geniculo-occipital (PGO) waves. Neuroscience 31:25–35PubMedCrossRefGoogle Scholar
  13. Ito K, McCarley RW (1987) Physiological studies of brainstem reticular connectivity. I. Responses of mPRF neurons to stimulation of bulbar reticular formation. Brain Res 409:97–110PubMedCrossRefGoogle Scholar
  14. Jouvet M (1962) Recherches sur les structures nerveuses et les mécanismes responsables des différentes phases du sommeil physiologique. Arch Ital Biol 100:125–206PubMedGoogle Scholar
  15. Kaneko CRS, Fuchs AF (1982) Mesencephalic neurons that discharge for target movements, saccades and eye position. Soc Neurosci Abstr 8:157Google Scholar
  16. Kang Y, Kitai ST (1990) Electrophysiological properties of pedunculopontine neurons and their postsynaptic responses following stimulation of substantia nigra reticulata. Brain Res (in press)Google Scholar
  17. Kleinschmidt A, Bear MF, Singer W (1987) Blockade of NMDA receptors disrupt experience-dependent plasticity of kitten striate cortex. 238:355–358Google Scholar
  18. Laurent JP, Alayaguerrero F (1975) Reversible suppression of ponto-geniculo-occipital waves by localized cooling during paradoxical sleep in cat. Exp Neurol 49:356–369PubMedCrossRefGoogle Scholar
  19. Laurent JP, Ayalaguerrero F, Jouvet M (1974a) Reversible suppression of the geniculate PGO waves and the concomitant increase of excitability of the intra-geniculate optic nerve terminals in cat. Brain Res 81:558–563PubMedCrossRefGoogle Scholar
  20. Laurent JP, Cespuglio R, Jouvet M (1974b) Délimitation des voies ascendantes de l'activité ponto-géniculo-occipitale chez le chat. Brain Res 65:29–52PubMedCrossRefGoogle Scholar
  21. Leonard CS, Llinás R (1988) Electrophysiology of thalamicprojecting cholinergic brainstem neurons and their inhibition by ACh. Soc Neurosci Abstr 14:297Google Scholar
  22. Matsumoto J, Jouvet M (1964) Effets de reserpine, DOPA et 5HTP sur les deux états de sommeil. C R Soc Biol (Paris) 158:2137–2140Google Scholar
  23. McCarley RW, Ito K (1983) Intracellular evidence linking medial pontine reticular formation neurons to PGO wave generation. Brain Res 280:343–348PubMedCrossRefGoogle Scholar
  24. McCarley RW, Ito K, Rodrigo-Angulo ML (1987) Physiological studies of brainstem reticular connectivity. II. Responses of mPRF neurons to stimulation of mesencephalic and contralateral pontine reticular formation. Brian Res 409:111–127CrossRefGoogle Scholar
  25. McCarley RW, Nelson JP, Hobson JA (1978) Ponto-geniculo-occipital (PGO) burst neurons: correlative evidence for neuronal generators of PGO waves. Science 201:269–272PubMedGoogle Scholar
  26. Mesulam MM (1982) Axonal transport enzyme histochemistry and light microscopic analysis. In: Mesulam MM (ed) Tracing neural connections with horseradish peroxidase. Wiley, New York, pp 1–151Google Scholar
  27. Nelson JP, McCarley RW, Hobson JA (1983) REM sleep burst neurons, PGO waves, and eye movement information. J Neurophysiol 50:784–797PubMedGoogle Scholar
  28. Noda T, Oka H (1984) Nigral inputs to the pedunculopontine region: intracellular analysis. Brain Res 322:223–227CrossRefGoogle Scholar
  29. Paré D, Smith Y, Parent A, Steriade M (1988) Projections of upper brainstem reticular cholinergic and non-cholinergic neurons of cat to intralaminar and reticular thalamic nuclei. Neuroscience 25:69–88PubMedCrossRefGoogle Scholar
  30. Ropert N, Steriade M (1981) Input-output organization of midbrain reticular core. J Neurophysiol 46:17–31PubMedGoogle Scholar
  31. Ruch-Monachon MA, Jalfre M, Haefly W (1976) Drugs and PGO waves in the lateral geniculate body of the curarized cat, I–IV. Arch Int Pharmacodyn 219:251–219PubMedGoogle Scholar
  32. Sakai K (1985) Anatomical and physiological basis of paradoxical sleep In: McGinty DJ, Morrison A, Drucker-Colin R, Parmeggiani PL (eds) Brain mechanisms of sleep. Raven, New York, pp 111–137Google Scholar
  33. Sakai K, Jouvet M (1980) Brain stem PGO-on cells projecting directly to the cat dorsal lateral geniculate nucleus. Brain Res 194:500–505PubMedCrossRefGoogle Scholar
  34. Sakai K, Petitjean F, Jouvet M (1976) Effects of pontomesencephalic lesions and electrical stimulation upon PGO waves and EMPs in unanesthetized cats. Electroencephalogr Clin Neurophysiol 41:49–63PubMedCrossRefGoogle Scholar
  35. Scarnati E, Proia A, Diloreto S, Pacitti C (1987) The reciprocal electrophysiological influence between the nucleus tegmenti pedunculopontinus and the substantia nigra in normal and decorticated rats. Brain Res 423:116–124PubMedCrossRefGoogle Scholar
  36. Schiller PH (1984) The superior colliculus and visual function. In: Darian-Smith I (ed) Handbook of physiology, Sect 1, Vol III. American Physiological Society, Bethesda, pp 457–505Google Scholar
  37. Smith Y, Paré D, Deschênes M, Parent A, Steriade M (1988) Cholinergic and non-cholinergic projections from the upper brainstem core to the visual thalamus in the cat. Exp Brain Res 70:166–180PubMedGoogle Scholar
  38. Sofroniew MV, Priestley JV, Consolazione A, Eckenstein F, Cuello AC (1985) Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res 329:213–223PubMedCrossRefGoogle Scholar
  39. Steriade M (1978) Cortical long-axoned cells and putative interneurons (with commentaries). Behav Brain Sci 3:465–514CrossRefGoogle Scholar
  40. Steriade M, Llinás R (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742PubMedGoogle Scholar
  41. Steriade M, McCarley RW (1990) Brainstem control of wakefulness and sleep. Plenum, New YorkGoogle Scholar
  42. Steriade M, Oakson G, Ropert N (1982) Firing rates and patterns of midbrain reticular neurons during steady and transitional states of the sleep-waking cycle. Exp Brain Res 46:37–51PubMedCrossRefGoogle Scholar
  43. Steriade M, Paré D (1990) Brainstem genesis and thalamic transfer of ponto-geniculo-occipital waves: cellular data and hypotheses. In: Montplaisir J, Godbout R (eds) Sleep and biological rhythms. Oxford University Press, New York Oxford pp 148–162Google Scholar
  44. Steriade M, Paré D, Parent A, Smith Y (1988) Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat macaque monkey. Neuroscience 25:47–67PubMedCrossRefGoogle Scholar
  45. Steriade M, Paré D, Bouhassira D, Deschênes M, Oakson G (1989) Phasic activation of lateral geniculate and perigeniculate thalamic neurons during sleep with ponto-geniculo-occipital waves. J Neurosci 9:2215–2229PubMedGoogle Scholar
  46. Steriade M, Paré D, Datta S, Oakson G, Curro Dossi R (1990) Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves. J Neurosci (in press)Google Scholar
  47. Vincent SR, Satoh K, Armstrong DM, Fibiger HC (1983) NADPH-DIAPHORASE: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci Lett 43:31–36PubMedCrossRefGoogle Scholar
  48. Waitzman DM (1983) Burst neurons in the mesencephalic reticular formation (MRF) of the rhesus monkey associated with saccadic eye movement. Thesis. New York UniversityGoogle Scholar
  49. Webster HH, Jones BE (1988) Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat: effects upon sleep-waking states. Brain Res 458:285–302PubMedCrossRefGoogle Scholar
  50. Woolf NJ, Butcher LL (1986) Cholinergic systems in the rat brain. III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and the basal forebrain. Brain Res Bull 16:603–637PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • D. Paré
    • 1
  • R. Curró Dossi
    • 1
  • S. Datta
    • 1
  • M. Steriade
    • 1
  1. 1.Laboratoire de Neurophysiologie, Faculté de MédecineUniversité LavalCanada

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