Differential modulation of high-frequency γ-electroencephalogram activity and sleep-wake state by noradrenaline and serotonin microinjections into the region of cholinergic basalis neurons

Journal of Neuroscience

Volumn 18, Issue 7, 1998, Pages 2653-2666

  Cape, Edmund G ^a   Jones, Barbara E ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Acetylcholine; Basal forebrain; Locus coeruleus; Paradoxical sleep; Raphe; Slow wave sleep; Waking

Indexed keywords

NORADRENALIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FOREBRAIN; LOCUS CERULEUS; MALE; NONHUMAN; NORADRENALIN RELEASE; PRIORITY JOURNAL; RAT; REM SLEEP; SEROTONIN RELEASE; SLOW WAVE SLEEP;

EID: 0032053956     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-07-02653.1998     Document Type: Article

References (56)

1. Aghajanian GK, Wang RY, Barban J (1978) Serotonergic and nonserotonergic neurons of the dorsal raphe: reciprocal changes in firing induced by peripheral nerve stimulation. Brain Res 153:169-175.
2. Aston-Jones G, Bloom FE (1981a) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1:876-886.
3. Aston-Jones G, Bloom FE (1981b) Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1:887-900.
4. Berridge CW, Foote SL (1991) Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. J Neurosci 11:3135-3145.
5. Buzsáki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH (1988) Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 8:4007-4026.
6. Cape E, Jones BE (1994) Modulation of sleep-wake state and cortical activity following injection of agonists into the region of cholinergic basal forebrain neurons. Soc Neurosci Abstr 20:156.
7. Casamenti F, Deffenu G, Abbamondi AL, Pepeu G (1986) Changes in cortical acetylcholine output induced by modulation of the nucleus basalis. Brain Res Bull 16:689-695.
8. Celesia GG, Jasper HH (1966) Acetylcholine released from cerebral cortex in relation to state of activation. Neurology 16:1053-1064.
9. Delagrange P, Tadjer D, Bouyer J-J, Rougeul A, Conrath M (1989) Effect of DSP4, a neurotoxic agent, on attentive behaviour and related electrocortical activity in cat. Behav Brain Res 33:33-43.
10. Denoyer M, Sallanon M, Kitahama K, Aubert C, Jouvet M (1989) Reversibility of para-chlorophenylalanine-induced insomnia by intrahypothalamic microinjection of L-5-hydroxytryptophan. Neuroscience 28:83-94.
11. Fornal CA, Metzler CW, Marrosu F, Ribiero-do-Valle LE, Jacobs BL (1996) A subgroup of dorsal raphe serotonergic neurons in the cat is strongly activated during oral-buccal movements. Brain Res 716:123-133.
12. Fort P, Khateb A, Alonso A, Jones BE, Muhlethaler M (1992) Pharmacological heterogeneity of basal forebrain neurones. Soc Neurosci Abstr 18:881.
13. Fort P, Khateb A. Pegna A, Muhlethaler M, Jones BE (1995) Noradrenergic modulation of cholinergic nucleus basalis neurons demonstrated by in vitro pharmacological and immunohistochemical evidence in the guinea pig brain. Eur J Neurosci 7:1502-1511.
14. Fort P, Khateb A, Serafin M, Muhlethaler M, Jones BE (1998) Pharmacological characterization and differentiation of non-cholinergic nucleus basalis neurons in vitro. NeuroReport. 9:61-65.
15. Gritti I, Mainville L, Jones BE (1993) Codistribution of GABA- with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J Comp Neurol 329:438-457.
16. Hobson JA, McCarley RW, Wyzinski PW (1975) Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189:55-58.
17. Holmes CJ, Jones BE (1994) Importance of cholinergic, GABAergic, serotonergic, and other neurons in the medullary reticular formation for sleep-wake states studied by cytotoxic lesions in the cat. Neuroscience 62:1179-1200.
18. Jacobs BL, Fornal CA (1991) Activity of brain serotonergic neurons in the behaving animal. Pharmacol Rev 43:563-578.
19. Jacobs BL, Jones BE (1978) The role of central monoamine and acetylcholine systems in sleep-wakefulness states: mediation or modulation. In: Cholinergic-monoaminergic interactions in the brain (Butcher LL, ed), pp 271-290. New York: Academic.
20. Jasper HH, Tessier J (1971) Acetylcholine liberation from cerebral cortex during paradoxical (REM) sleep. Science 172:601-602.
21. Jones BE (1991) The role of noradrenergic locus coeruleus neurons and neighboring cholinergic neurons of the pontomesencephalic tegmentum in sleep-wake states. In: Neurobiology of the locus coeruleus. Progress in brain research, Vol 85 (Barnes C, Pompeiano O, eds), pp 532-543. Amsterdam: Elsevier.
22. Jones BE (1993) The organization of central cholinergic systems and their functional importance in sleep-waking states. In: Cholinergic function and dysfunction. Progress in brain research, Vol 98 (Cuello AC, ed), pp 61-71. Amsterdam: Elsevier.
23. Jones BE (1994) Basic mechanisms of sleep-wake states. In: Principles and practice of sleep medicine, 2nd Ed (Kryger MH, Roth T, Dement WC, eds), pp 145-162. Philadelphia: Saunders.
24. Jones BE (1995) Reticular formation. Cytoarchkecture, transmitters, and projections. In: The rat nervous system, 2nd Ed (Paxinos G, ed), pp 155-171. New South Wales, Australia: Academic.
25. 3H]choline into the forebrain of the rat. Exp Brain Res 65:437-448.
26. Jones BE, Cuello AC (1989) Afferents to the basal forebrain cholinergic cell area from pontomesencephalic - catecholamine, serotonin, and acetylcholine - neurons. Neuroscience 31:37-61.
27. Jones BE, Yang T-Z (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56-92.
28. Jones BE, Bobillier P, Pin C, Jouvet M (1973) The effect of lesions of catecholamine-containing neurons upon monoamine content of the brain and EEG and behavioral waking in the cat. Brain Res 58:157-177.
29. Jones BE, Harper ST, Halaris AE (1977) Effects of locus coeruleus lesions upon cerebral monoamine content, sleep-wakefulness states and the response to amphetamine. Brain Res 124:473-496.
30. Jouvet M (1972) The role of monoamines and acetylcholine-containing neurons in the regulation of the sleep-waking cycle. Ergeb Physiol 64:165-307.
31. Khateb A, Muhlethaler M, Alonso A, Serafin M, Mainville L, Jones BE (1992) Cholinergic nucleus basalis neurons display the capacity for rhythmic bursting activity mediated by low threshold calcium spikes. Neuroscience 51:489-494.
32. Khateb A, Fort P, Alonso A, Jones BE, Muhlethaler M (1993) Pharmacological and immunohistochemical evidence for a serotonergic input to cholinergic nucleus basalis neurons. Eur J Neurosci 5:541-547.
33. Krnjevic K (1967) Chemical transmission and cortical arousal. Anesthesiology 28:100-104.
34. Lehmann J, Nagy JI, Atmadja S, Fibiger HC (1980) The nucleus basalis magnocellularis: the origin of a cholinergic projection to the neocortex of the rat. Neuroscience 5:1161-1174.
35. Lo Conte G, Casamenti F, Bigl V, Milaneschi E, Pepeu G (1982) Effect of magnocellular forebrain nuclei lesions on acetylcholine output from the cerebral cortex, electrocorticogram, and behaviour. Arch Ital Biol 120:176-188.
36. Longo VG (1966) Behavioral and electroencephalographic effects of atropine and related compounds. Pharmacol Rev 18:965-996.
37. Maloney KJ, Cape EG, Gotman J, Jones BE (1997) High frequency gamma electroencephalogram activity in association with sleep-wake states and spontaneous behaviors in the rat. Neuroscience 76:541-555.
38. Martin JH (1991) Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci Lett 127:160-164.
39. McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39:337-388.
40. McGinty D, Harper RM (1976) Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 101:569-575.
41. Metherate R, Cox CL, Ashe JH (1992) Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12:4701-4711.
42. Moruzzi G, Magoun HW (1949) Brainstem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1:455-473.
43. Myers RD (1974) Handbook of drug and chemical stimulation of the brain. New York: Van Nostrand Reinhold.
44. Rasmusson DD, Clow K, Szerb JC (1994) Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain. Neuroscience 60:665-677.
45. Rasmussen K, Morilak DA, Jacobs BL (1986) Single unit activity of locus coeruleus neurons in the freely moving cat. I. During naturalistic behaviors and in response to simple and complex stimuli. Brain Res 371:324-334.
46. Rye DB, Wainer BH, Mesulam M-M, Mufson EJ, Saper CB (1984) Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13:627-643.
47. Semba K, Reiner PB, McGeer EG, Fibiger HC (1988) Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 267:433-453.
48. Shute CCD, Lewis PR (1967) The ascending cholinergic reticular system: neocortical, olfactory, and subcortical projections. Brain 90:497-520.
49. Starzl TE, Taylor CW, Magoun HW (1951) Ascending conduction in reticular activating system, with special reference to the diencephalon. J Neurophysiol 14:461-477.
50. Steriade M, Hobson JA (1976) Neuronal activity during the sleep-waking cycle. Prog Neurobiol 6:155-376.
51. Stewart DJ, Macfabe DF, Vanderwolf CH (1984) Cholinergic activation of the electrocorticogram: role of the substantia innominata and effects of atropine and quinuclidinyl benzilate. Brain Res 322:219-232.
52. Swanson LW, Mogenson GJ, Gerfen CR, Robinson P (1984) Evidence for a projection from the lateral preoptic area and substantia innominata to the "mesencephalic locomotor region" in the rat. Brain Res 295:161-178.
53. Trulson ME, Jacobs BL (1979) Raphe unit activity in freely moving cats: correlation with level of behavioral arousal. Brain Res 163:135-150.
54. Vergnes M, Marescaux C, Micheletti G, Reis J, Depaulis A, Rumbach L, Warter JM (1982) Spontaneous paroxysmal electroclinical patterns in rat: a model of generalized non-convulsive epilepsy. Neurosci Lett 33:97-101.
55. 1A agonists, 8-OH-DPAT and buspirone, produces hippocampal theta rhythm in the rat. Neuroscience 60:441-451.
56. Wenk GL (1984) Pharmacological manipulations of the substantia innominata-cortical cholinergic pathway. Neurosci Lett 51:99-103.