The role of GABAergic modulation of mesopontine cholinergic neurotransmission in rapid eye movement (REM) sleep

GABA and Sleep: Molecular, Functional and Clinical Aspects

Volumn 9783034602266, Issue , 2010, Pages 253-277

  Marks, Gerald A ^a,b   Sinton, Christopher M ^b  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79955011806     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-0346-0226-6_12     Document Type: Chapter

References (92)

1. Dement W (1958) The occurrence of low voltage, fast, electroencephalogram patterns during behavioral sleep in the cat. Electroencephalogr Clin Neurophysiol 10:291-296
2. Jouvet M (1962) Research on the neural structures and responsible mechanisms in different phases of physiological sleep. Arch Ital Biol 100:125-206
3. Vanni-Mercier G, Sakai K, Lin JS, Jouvet M (1991) Carbachol microinjections in the mediodorsal pontine tegmentum are unable to induce paradoxical sleep after caudal pontine and prebulbar transections in the cat. Neurosci Lett 130:41-45
4. Webster HH, Friedman L, Jones BE (1986) Modification of paradoxical sleep following transections of the reticular formation at the pontomedullary junction. Sleep 9:1-23
5. Siegel JM, Nienhuis R, Tomaszewski KS (1984) REM sleep signs rostral to chronic transections at the pontomedullary junction. Neurosci Lett 45:241-246
6. Wurts SW, Edgar DM (2000) Circadian and homeostatic control of rapid eye movement (REM) sleep: promotion of REM tendency by the suprachiasmatic nucleus. J Neurosci 20:4300-4310
7. Jouvet M (1965) Paradoxical sleep - a study of Its nature and mechanisms. Prog Brain Res 18:20-62
8. Jouvet M (1988) The regulation of paradoxical sleep by the hypothalamo-hypophysis. Arch Ital Biol 126:259-274
9. Vertes RP (1984) Brainstem control of the events of REM sleep. Prog Neurobiol 22:241-288
10. Webster HH, Jones BE (1988) Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat. II. Effects upon sleep-waking states. Brain Res 458:285-302
11. Shute CC, Lewis PR (1967) The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. Brain 90:497-520
12. George R, Haslett WL, Jenden DJ (1964) A cholinergic mechanism in the brainstem reticular formation: induction of paradoxical sleep. Int J Neuropharmacol 3:541-552
13. Reinoso-Suarez F, De Andres I, Rodrigo-Angulo ML, Rodriguez-Veiga E (1994) Location and anatomical connections of a paradoxical sleep induction site in the cat ventral pontine tegmentum. Eur J Neurosci 6:1829-1836
14. Baghdoyan HA, Rodrigo-Angulo ML, McCarley RW, Hobson JA (1987) A neuroanatomical gradient in the pontine tegmentum for the cholinoceptive induction of desynchronized sleep signs. Brain Res 414:245-261
15. Vanni-Mercier G, Sakai K, Lin JS, Jouvet M (1989) Mapping of cholinoceptive brainstem structures responsible for the generation of paradoxical sleep in the cat. Arch Ital Biol 127:133-164
16. Yamamoto K, Mamelak AN, Quattrochi JJ, Hobson JA (1990) A cholinoceptive desynchronized sleep induction zone in the anterodorsal pontine tegmentum: spontaneous and druginduced neuronal activity. Neuroscience 39:295-304
17. Mitler MM, Dement WC (1974) Cataplectic-like behavior in cats after micro-injections of carbachol in pontine reticular formation. Brain Res 68:335-343
18. Sakai K (1985) Anatomical and physiological basis of paradoxical sleep. In: McGinty DJ, Drucker-Colin R, Morrison AR, Parmeggiani PL (eds) Brain mechanisms of sleep. Raven, New York, pp 111-138
19. Datta S, Hobson JA (1995) Suppression of ponto-geniculo-occipital waves by neurotoxic lesions of pontine caudo-lateral peribrachial cells. Neuroscience 67:703-712
20. Garzon M, De Andres I, Reinoso-Suarez F (1998) Sleep patterns after carbachol delivery in the ventral oral pontine tegmentum of the cat. Neuroscience 83:1137-1144
21. Shouse MN, Siegel JM (1992) Pontine regulation of REM sleep components in cats: integrity of the pedunculopontine tegmentum (PPT) is important for phasic events but unnecessary for atonia during REM sleep. Brain Res 571:50-63
22. Jones BE (1990) Immunohistochemical study of choline acetyltransferase-immunoreactive processes and cells innervating the pontomedullary reticular formation in the rat. J Comp Neurol 295:485-514
23. Satoh K, Fibiger HC (1986) Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J Comp Neurol 253:277-302
24. Semba K (1993) Aminergic and cholinergic afferents to REM sleep induction regions of the pontine reticular formation in the rat. J Comp Neurol 330:543-556
25. Luppi PH, Sakai K, Fort P, Salvert D, Jouvet M (1988) The nuclei of origin of monoaminergic, peptidergic, and cholinergic afferents to the cat nucleus reticularis magnocellularis: a doublelabeling study with cholera toxin as a retrograde tracer. J Comp Neurol 277:1-20
26. Reiner PB, Vincent SR (1987) Topographic relations of cholinergic and noradrenergic neurons in the feline pontomesencephalic tegmentum: an immunohistochemical study. Brain Res Bull 19:705-714
27. el Mansari M, Sakai K, Jouvet M (1989) Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 76:519-529
28. Koyama Y, Kayama Y, Sakai K (1999) Different physiological properties of two populations of PS-on neurons in the mesopontine tegmentum. In: Mallick BN, Inoue S (eds) Rapid eye movement sleep. Marcel Dekker, New York, pp 221-232
29. Kodama T, Takahashi Y, Honda Y (1990) Enhancement of acetylcholine release during paradoxical sleep in the dorsal tegmental field of the cat brain stem. Neurosci Lett 114:277-282
30. McCarley RW, Hobson JA (1975) Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 189:58-60
31. Hobson JA, McCarley RW, Wyzinski PW (1975) Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 189:55-58
32. Vivaldi E, McCarley RW, Hobson JA (1980) Evocation of desynchronized sleep signs by chemical microstimulation of the pontine brain stem. In: Hobson JA, Brazier MAB (eds) The reticular formation revisited. Raven, New York, pp 513-529
33. Muhlethaler M, Khateb A, Serafin M (1990) Effects of monoamines and opiates on pedunculopontine neurons. In: Mancia M, Marini G (eds) The diencephalon and sleep. Raven, New York, pp 367-378
34. Luebke JI, Greene RW, Semba K, Kamondi A, McCarley RW, Reiner PB (1992) Serotonin hyperpolarizes cholinergic low-threshold burst neurons in the rat laterodorsal tegmental nucleus in vitro. Proc Natl Acad Sci USA 89:743-747
35. Leonard CS, Llinas R (1994) Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study. Neuroscience 59:309-330
36. Williams JA, Reiner PB (1993) Noradrenaline hyperpolarizes identified rat mesopontine cholinergic neurons in vitro. J Neurosci 13:3878-3883
37. Kohlmeier KA, Reiner PB (1999) Noradrenaline excites non-cholinergic laterodorsal tegmental neurons via two distinct mechanisms. Neuroscience 93:619-630
38. el Mansari M, Sakai K, Jouvet M (1990) Responses of presumed cholinergic mesopontine tegmental neurons to carbachol microinjections in freely moving cats. Exp Brain Res 83:115-123
39. Sakai K, Onoe H (1997) Critical role for M3 muscarinic receptors in paradoxical sleep generation in the cat. Eur J Neurosci 9:415-423
40. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56:615-649
41. Baghdoyan HA, Lydic R (1992) M2 muscarinic receptor subtype in the feline medial pontine reticular formation modulates the amount of rapid eye movement sleep. Sleep 22:835-847
42. Lancel M (1999) Role of GABAA receptors in the regulation of sleep: initial sleep responses to peripherally administered modulators and agonists. Sleep 22:33-42
43. Xi MC, Morales FR, Chase MH (1999) A GABAergic pontine reticular system is involved in the control of wakefulness and sleep. Sleep Res Online 2:43-48
44. Xi MC, Morales FR, Chase MH (1999) Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J Neurophysiol 82:2015-2019
45. Vazquez J, Baghdoyan HA (2004) GABAA receptors inhibit acetylcholine release in cat pontine reticular formation: implications for REM sleep regulation. J Neurophysiol 92:2198-2206
46. Xi MC, Morales FR, Chase MH (2004) Interactions between GABAergic and cholinergic processes in the nucleus pontis oralis: neuronal mechanisms controlling active (rapid eye movement) sleep and wakefulness. J Neurosci 24:10670-10678
47. Petitjean F, Sakai K, Blondaux C, Jouvet M (1975) Hypersomnia by isthmic lesion in cat. II. Neurophysiological and pharmacological study. Brain Res 88:439-453
48. Sastre JP, Buda C, Kitahama K, Jouvet M (1996) Importance of the ventrolateral region of the periaqueductal gray and adjacent tegmentum in the control of paradoxical sleep as studied by muscimol microinjections in the cat. Neuroscience 74:415-426
49. Bourgin P, Escourrou P, Gaultier C, Adrien J (1995) Induction of rapid eye movement sleep by carbachol infusion into the pontine reticular formation in the rat. NeuroReport 6:532-536
50. Marks GA, Birabil CG (1998) Enhancement of rapid eye movement sleep in the rat by cholinergic and adenosinergic agonists infused into the pontine reticular formation. Neuroscience 86:29-37
51. Marks GA, Birabil CG (2001) Comparison of three muscarinic agonists injected into the medial pontine reticular formation of rats to enhance REM sleep. Sleep Res Online 4:17-24
52. Marks GA, Shaffery JP, Speciale SG, Birabil CG (2003) Enhancement of rapid eye movement sleep in the rat by actions at A1 and A2a adenosine receptor subtypes with a differential sensitivity to atropine. Neuroscience 116:913-920
53. Ahnaou A, Basille M, Gonzalez B, Vaudry H, Hamon M, Adrien J, Bourgin P (1999) Longterm enhancement of REM sleep by the pituitary adenylyl cyclase-activating polypeptide (PACAP) in the pontine reticular formation of the rat. Eur J Neurosci 11:4051-4058
54. Ahnaou A, Laporte AM, Ballet S, Escourrou P, Hamon M, Adrien J, Bourgin P (2000) Muscarinic and PACAP receptor interactions at pontine level in the rat: significance for REM sleep regulation. Eur J Neurosci 12:4496-4504
55. Bourgin P, Ahnaou A, Laporte AM, Hamon M, Adrien J (1999) Rapid eye movement sleep induction by vasoactive intestinal peptide infused into the oral pontine tegmentum of the rat may involve muscarinic receptors. Neuroscience 89:291-302
56. Bier MJ, McCarley RW (1994) REM-enhancing effects of the adrenergic antagonist idazoxan infused into the medial pontine reticular formation of the freely moving cat. Brain Res 634:333-338
57. Yamuy J, Morales FR, Chase MH (1995) Induction of rapid eye movement sleep by the microinjection of nerve growth factor into the pontine reticular formation of the cat. Neuroscience 66:9-13
58. Sanford LD, Tang X, Xiao J, Ross RJ, Morrison AR (2003) GABAergic regulation of REM sleep in reticularis pontis oralis and caudalis in rats. J Neurophysiol 90:938-945
59. Deurveilher S, Hars B, Hennevin E (1997) Pontine microinjection of carbachol does not reliably enhance paradoxical sleep in rats. Sleep 20:593-607
60. Marks GA, Birabil CG (2007) Carbachol induction of REM sleep in the rat is more effective at lights-out than lights-on. Brain Res 1142:127-134
61. Marks GA, Birabil CG (2000) Infusion of adenylyl cyclase inhibitor SQ22, 536 into the medial pontine reticular formation of rats enhances rapid eye movement sleep. Neuroscience 98:311-315
62. Bandyopadhya RS, Datta S, Saha S (2006) Activation of pedunculopontine tegmental protein kinase A: a mechanism for rapid eye movement sleep generation in the freely moving rat. J Neurosci 26:8931-8942
63. Greene RW, Gerber U, McCarley RW (1989) Cholinergic activation of medial pontine reticular formation neurons in vitro. Brain Res 476:154-159
64. Gerber U, Stevens DR, McCarley RW, Greene RW (1991) Muscarinic agonists activate an inwardly rectifying potassium conductance in medial pontine reticular formation neurons of the rat in vitro. J Neurosci 11:3861-3867
65. Brown RE, McKenna JT, Winston S, Basheer R, Yanagawa Y, Thakkar MM, McCarley RW (2008) Characterization of GABAergic neurons in rapid-eye-movement sleep controlling regions of the brainstem reticular formation in GAD67-green fluorescent protein knock-in mice. Eur J Neurosci 27:352-363
66. Coleman CG, Lydic R, Baghdoyan HA (2004) M2 muscarinic receptors in pontine reticular formation of C57BL/6J mouse contribute to rapid eye movement sleep generation. Neuroscience 126:821-830
67. Caulfield MP (1993) Muscarinic receptors - characterization, coupling and function. Pharmacol Ther 58:319-379
68. Goutagny R, Comte JC, Salvert D, Gomeza J, Yamada M, Wess J, Luppi PH, Fort P (2005) Paradoxical sleep in mice lacking M3 and M2/M4 muscarinic receptors. Neuropsychobiology 52:140-146
69. Deurveilher S, Hennevin E (2001) Lesions of the pedunculopontine tegmental nucleus reduce paradoxical sleep (PS) propensity: evidence from a short-term PS deprivation study in rats. Eur J Neurosci 13:1963-1976
70. Marks GA, Sachs OW, Birabil CG (2008) Blockade of GABA, type A, receptors in the rat pontine reticular formation induces rapid eye movement sleep that is dependent upon the cholinergic system. Neuroscience 156:1-10
71. Flint RR, Lydic R, Baghdoyan HA (2009) Microdialysis delivery of the GABA-A receptor antagonist bicuculline to the pontine reticular formation (PRF) of C57BL/6J (B6) mouse increases PRF acetylcholine (ACh) release, Program #375.12. Neuroscience Meeting Planner, Society for Neuroscience, Chicago, Online
72. A receptors located on cholinergic terminals in the nucleus pontis oralis of the rat: implications for REM sleep control
73. Kayama Y, Ohta M, Jodo E (1992) Firing of 'possibly' cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness. Brain Res 569:210-220
74. Datta S, Siwek DF (2002) Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats. J Neurosci Res 70:611-621
75. Swanson LW (2003) Brain maps: structure of the rat brain, 3rd edn. Elsevier, New York
76. Boissard R, Gervasoni D, Schmidt MH, Barbagli B, Fort P, Luppi PH (2002) The rat pontomedullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study. Eur J Neurosci 16:1959-1973
77. Pollock MS, Mistlberger RE (2003) Rapid eye movement sleep induction by microinjection of the GABA-A antagonist bicuculline into the dorsal subcoeruleus area of the rat. Brain Res 962:68-77
78. Datta S, Siwek DF, Patterson EH, Cipolloni PB (1998) Localization of pontine PGO wave generation sites and their anatomical projections in the rat. Synapse 30:409-423
79. Luppi PH, Gervasoni D, Verret L, Goutagny R, Peyron C, Salvert D, Leger L, Fort P (2007) Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergicglutamatergic hypothesis. J Physiol 100:271-283
80. Lu J, Sherman D, Devor M, Saper CB (2006) A putative flip-flop switch for control of REM sleep. Nature 441:589-594
81. Fort P, Bassetti CL, Luppi PH (2009) Alternating vigilance states: new insights regarding neuronal networks and mechanisms. Eur J Neurosci 29:1741-1753
82. Vetrivelan R, Fuller PM, Tong Q, Lu J (2009) Medullary circuitry regulating rapid eye movement sleep and motor atonia. J Neurosci 29:9361-9369
83. Sapin E, Lapray D, Berod A, Goutagny R, Leger L, Ravassard P, Clement O, Hanriot L, Fort P, Luppi PH (2009) Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS ONE 4:e4272
84. Boissard R, Fort P, Gervasoni D, Barbagli B, Luppi PH (2003) Localization of the GABAergic and non-GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur J Neurosci 18:1627-1639
85. Herdegen T, Leah JD (1998) Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Rev 28:370-490
86. Sheng M, Greenberg ME (1990) The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477-485
87. Maloney KJ, Mainville L, Jones BE (1999) Differential c-Fos expression in cholinergic, monoaminergic, and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J Neurosci 19:3057-3072
88. Maloney KJ, Mainville L, Jones BE (2000) c-Fos expression in GABAergic, serotonergic, and other neurons of the pontomedullary reticular formation and raphe after paradoxical sleep deprivation and recovery. J Neurosci 20:4669-4679
89. Vanini G, Torterolo P, McGregor R, Chase MH, Morales FR (2007) GABAergic processes in the mesencephalic tegmentum modulate the occurrence of active (rapid eye movement) sleep in guinea pigs. Neuroscience 145:1157-1167
90. Datta S, Siwek DF, Stack EC (2009) Identification of cholinergic and non-cholinergic neurons in the pons expressing phosphorylated cyclic adenosine monophosphate response elementbinding protein as a function of rapid eye movement sleep. Neuroscience 163:397-414
91. Clement O, Sapin E, Berod A, Gervasoni D, Fort P, Luppi PH (2009) Evidence that neurons of the sublaterodorsal tegmental nucleus triggering paradoxical (REM) sleep are glutamatergic, Program #375.21. Neuroscience Meeting Planner, Society for Neuroscience, Chicago, Online
92. Sanford LD, Tang X, Xiao J, Ross RJ, Morrison AR (2001) Sleep and behavior in rats with pontine lesions producing REM without atonia. Sleep Res Online 4:1-5