Noradrenergic neurons expressing Fos during waking and paradoxical sleep deprivation in the rat

Journal of Chemical Neuroanatomy

Volumn 37, Issue 3, 2009, Pages 149-157

  Léger, Lucienne ^a,b,c,d   Goutagny, Romain ^a,b,c,d   Sapin, Emilie ^a,b,c,d   Salvert, Denise ^a,b,c,d   Fort, Patrice ^a,b,c,d   Luppi, Pierre Hervé ^a,b,c,d  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CNRS   (France)

^d CNRS UMR5167   (France)

Author keywords

Double labeling; Immunohistochemistry; Noradrenaline; Novel environment; Paradoxical sleep recovery

Indexed keywords

NORADRENALIN; PROTEIN FOS; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN STEM; CHEMICAL LABELING; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LOCUS CERULEUS; MALE; NERVE STIMULATION; NONHUMAN; NORADRENERGIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REM SLEEP; SLEEP DEPRIVATION; SLEEP WAKING CYCLE; WAKEFULNESS;

ANIMALS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; NOREPINEPHRINE; ONCOGENE PROTEINS V-FOS; RATS; SLEEP DEPRIVATION; SLEEP, REM; TYROSINE 3-MONOOXYGENASE;

EID: 60949093033     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2008.12.008     Document Type: Article

References (73)

1. Arluison M., Dietl M., and Thibault J. Ultrastructural morphology of dopaminergic nerve terminals and synapses in the striatum of the rat using tyrosine hydroxylase immunocytochemistry: a topographical study. Brain Res. Bull. 13 (1984) 269-285
2. Aston-Jones G., and Bloom F.E. Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J. Neurosci. 1 (1981) 887-900
3. Aston-Jones G., and Bloom F.E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J. Neurosci. 1 (1981) 876-886
4. Aston-Jones G., and Cohen J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28 (2005) 403-450
5. Berridge C.W., and Waterhouse B.D. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Brain Res. Rev. 42 (2003) 33-84
6. Boissard R., Gervasoni D., Schmidt M.H., Barbagli B., Fort P., and Luppi P.H. The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study. Eur. J. Neurosci. 16 (2002) 1959-1973
7. Bouret S., and Sara S.J. Network reset: a simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 28 (2005) 574-582
8. Brett L.P., Chong G.S., Coyle S., and Levine S. The pituitary-adrenal response to novel stimulation and ether stress in young adult and aged rats. Neurobiol. Aging 4 (1983) 133-138
9. Brock J.W., Farooqui S.M., Ross K.D., Payne S., and Prasad C. Stress-related behavior and central norepinephrine concentrations in the REM sleep-deprived rat. Physiol. Behav. 55 (1994) 997-1003
10. Byrum C.E., and Guyenet P.G. Afferent and efferent connections of the A5 noradrenergic cell group in the rat. J. Comp. Neurol. 261 (1987) 529-542
11. Chen X., and Herbert J. Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlations with cardiovascular, hypothermic and endocrine responses. Neuroscience 64 (1995) 675-685
12. Cohen R.M., Pickar D., Garnett D., Lipper S., Gillin J.C., and Murphy D.L. REM sleep suppression induced by selective monoamine oxidase inhibitors. Psychopharmacology (Berl) 78 (1982) 137-140
13. Crochet S., and Sakai K. Alpha-2 adrenoceptor mediated paradoxical (REM) sleep inhibition in the cat. Neuroreport 10 (1999) 2199-2204
14. Dahlström A., and Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand. (Suppl.) 232 (1964) 1-55
15. Deurveilher S., Lo H., Murphy J.A., Burns J., and Semba K. Differential c-Fos immunoreactivity in arousal-promoting cell groups following systemic administration of caffeine in rats. J. Comp. Neurol. 498 (2006) 667-689
16. Dragunow M., and Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 29 (1989) 261-265
17. Erickson J.T., and Millhorn D.E. Hypoxia and electrical stimulation of the carotid sinus nerve induce Fos-like immunoreactivity within catecholaminergic and serotoninergic neurons of the rat brainstem. J. Comp. Neurol. 348 (1994) 161-182
18. Fenik V., Marchenko V., Janssen P., Davies R.O., and Kubin L. A5 cells are silenced when REM sleep-like signs are elicited by pontine carbachol. J. Appl. Physiol. 93 (2002) 1448-1456
19. Franken P. Long-term vs. short-term processes regulating REM sleep. J. Sleep Res. 11 (2002) 17-28
20. Gervasoni D., Darracq L., Fort P., Souliere F., Chouvet G., and Luppi P.H. Electrophysiological evidence that noradrenergic neurons of the rat locus coeruleus are tonically inhibited by GABA during sleep. Eur. J. Neurosci. 10 (1998) 964-970
21. Gervasoni D., Panconi E., Henninot V., Boissard R., Barbagli B., Fort P., and Luppi P.H. Effect of chronic treatment with milnacipran on sleep architecture in rats compared with paroxetine and imipramine. Pharmacol. Biochem. Behav. 73 (2002) 557-563
22. Glavin G.B. Stress and brain noradrenaline: a review. Neurosci. Biobehav. Rev. 9 (1985) 233-243
23. Graham J.C., Hoffman G.E., and Sved A.F. c-Fos expression in brain in response to hypotension and hypertension in conscious rats. J. Auton. Nerv. Syst. 55 (1995) 92-104
24. Han F., Zhang Y.F., and Li Y.Q. Fos expression in tyrosine hydroxylase-containing neurons in rat brainstem after visceral noxious stimulation: an immunohistochemical study. World J. Gastroenterol. 9 (2003) 1045-1050
25. 2-induced c-fos expression in the CNS catecholaminergic neurons. Respir. Physiol. 105 (1996) 35-45
26. Herbert H., and Saper C.B. Organization of medullary adrenergic and noradrenergic projections to the periaqueductal gray matter in the rat. J. Comp. Neurol. 315 (1992) 34-52
27. Hökfelt T., Martensson R., Björklund A., Kleinau S., and Goldstein M. Distribution maps of tyrosine-hydroxylase-immunoreactive neurons in the rat brain. In: Björklund H.T.A. (Ed). Handbook of Chemical Neuroanatomy vol. 2 (1984), Elsevier Science Publishers BV 277-287
28. Jacobs B.L. Single unit activity of locus coeruleus neurons in behaving animals. Prog. Neurobiol. 27 (1986) 183-194
29. Jobert M., Jahnig P., and Schulz H. Effect of two antidepressant drugs on REM sleep and EMG activity during sleep. Neuropsychobiology 39 (1999) 101-109
30. Jones B.E. Paradoxical sleep and its chemical/structural substrates in the brain. Neuroscience 40 (1991) 637-656
31. Jones B.E. From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol. Sci. 26 (2005) 578-586
32. Jouvet M. Biogenic amines and the states of sleep. Science 163 (1969) 32-41
33. Kovacs K.J. c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem. Int. 33 (1998) 287-297
34. Kovalzon V.M., and Tsibulsky V.L. REM-sleep deprivation, stress and emotional behavior in rats. Behav. Brain Res. 14 (1984) 235-245
35. Koyama Y., Takahashi K., Kodama T., and Kayama Y. State-dependent activity of neurons in the perifornical hypothalamic area during sleep and waking. Neuroscience 119 (2003) 1209-1219
36. Léger L., Goutagny R., Sapin E., Salvert D., Gervasoni D., Fort P., and Luppi P. Comparison of Fos expression in catecholaminergic neurons after paradoxical sleep deprivation/recovery and forced wakefulness in the rat. SfN (2006) (Abstract)
37. Léger L., Goutagny R., Sapin E., Salvert D., Fort P., and Luppi P. Comparison of Fos expression in catecholaminergic neurons after paradoxical sleep deprivation/recovery and forced wakefulness in the rat. Soc. Neurosci. (2007) (Abstract)
38. Lindvall O., and Björklund A. Dopamine- and norepinephrine-containing neuron systems: their anatomy in the rat brain. In: PC E. (Ed). Chemical Neuroanatomy (1983), Raven Press, New York pp. 229-255
39. Lu J., Jhou T.C., and Saper C.B. Identification of wake-active dopaminergic neurons in the ventral periaqueductal gray matter. J. Neurosci. 26 (2006) 193-202
40. Lu J., Sherman D., Devor M., and Saper C.B. A putative flip-flop switch for control of REM sleep. Nature 441 (2006) 589-594
41. Luppi P.H., Gervasoni D., Verret L., Goutagny R., Peyron C., Salvert D., Léger L., and Fort P. Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J. Physiol. Paris 100 (2006) 271-283
42. Maloney K.J., Mainville L., and Jones B.E. Differential c-Fos expression in cholinergic, monoaminergic, and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J. Neurosci. 19 (1999) 3057-3072
43. Maloney K.J., Mainville L., and Jones B.E. 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 (2000) 4669-4679
44. Marquez C., Nadal R., and Armario A. Influence of reactivity to novelty and anxiety on hypothalamic-pituitary-adrenal and prolactin responses to two different novel environments in adult male rats. Behav. Brain Res. 168 (2006) 13-22
45. Mendelson W.B., Cohen R.M., Campbell I.C., Murphy D.L., Gillin J.C., and Wyatt R.J. Lifetime monoamine oxidase inhibition and sleep. Pharmacol. Biochem. Behav. 16 (1982) 429-431
46. Merchant-Nancy H., Vazquez J., Aguilar-Roblero R., and Drucker-Colin R. c-fos proto-oncogene changes in relation to REM sleep duration. Brain Res. 579 (1992) 342-346
47. Merchant-Nancy H., Vazquez J., Garcia F., and Drucker-Colin R. Brain distribution of c-fos expression as a result of prolonged rapid eye movement (REM) sleep period duration. Brain Res. 681 (1995) 15-22
48. Modirrousta M., Mainville L., and Jones B.E. Orexin and MCH neurons express c-Fos differently after sleep deprivation vs. recovery and bear different adrenergic receptors. Eur. J. Neurosci. 21 (2005) 2807-2816
49. Morgan J.I., and Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 14 (1991) 421-451
50. Nishino S., and Mignot E. Pharmacological aspects of human and canine narcolepsy. Prog. Neurobiol. 52 (1997) 27-78
51. Nygren L.G., and Olson L. Intracisternal neurotoxins and monoamine neurons innervating the spinal cord: acute and chronic effects on cell and axon counts and nerve terminal densities. Histochemistry 52 (1977) 281-306
52. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1997), Academic Press, Sydney, Orlando
53. Riche D., De Pommery J., and Menetrey D. Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J. Comp. Neurol. 293 (1990) 399-424
54. Ross R.J., Gresch P.J., Ball W.A., Sanford L.D., and Morrison A.R. REM sleep inhibition by desipramine: evidence for an alpha-1 adrenergic mechanism. Brain Res. 701 (1995) 129-134
55. Roth K.A., and Katz R.J. Stress, behavioral arousal, and open field activity-a reexamination of emotionality in the rat. Neurosci. Biobehav. Rev. 3 (1979) 247-263
56. Rukhadze I., Fenik V.B., Branconi J.L., and Kubin L. Fos expression in pontomedullary catecholaminergic cells following rapid eye movement sleep-like episodes elicited by pontine carbachol in urethane-anesthetized rats. Neuroscience 152 (2008) 208-222
57. Sakai K., Sastre J.P., Kanamori N., and Jouvet M. State-specific neurones in the ponto-medullary reticular formation with special reference to the postural atonia during paradoxical sleep in the cat. In: Pompeiano O., and AimoneMarsan C. (Eds). Brain Mechanisms of Perceptual Awareness and Purposeful Behavior (1981), Raven Press, New York 405-429
58. Sakai K. Physiological properties and afferent connections of the locus coeruleus and adjacent tegmental neurons involved in the generation of paradoxical sleep in the cat. Prog. Brain Res. 88 (1991) 31-45
59. Sakai K., and Crochet S. Role of the locus coeruleus in the control of paradoxical sleep generation in the cat. Arch. Ital. Biol. 142 (2004) 421-427
60. Sastre J.P., Buda C., Kitahama K., and Jouvet M. 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 (1996) 415-426
61. Senba E., and Ueyama T. Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat. Neurosci. Res. 29 (1997) 183-207
62. Shiromani P.J., Malik M., Winston S., and McCarley R.W. Time course of Fos-like immunoreactivity associated with cholinergically induced REM sleep. J. Neurosci. 15 (1995) 3500-3508
63. Sinha A.K., Ciaranello R.D., Dement W.C., and Barchas J.D. Tyrosine hydroxylase activity in rat brain following "REM" sleep deprivation. J. Neurochem. 20 (1973) 1289-1290
64. Stamp J.A., and Herbert J. Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress. Neuroscience 94 (1999) 1313-1322
65. Swanson L.W. Brain Maps: Structure of the Rat Brain: a Laboratory Guide with Printed and Electronic Templates for Data, Models, and Schematics (1998), Elsevier, New York
66. Verret L., Goutagny R., Fort P., Cagnon L., Salvert D., Léger L., Boissard R., Salin P., Peyron C., and Luppi P.H. A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neurosci. 4 (2003) 19
67. Verret L., Léger L., Fort P., and Luppi P.H. Cholinergic and noncholinergic brainstem neurons expressing Fos after paradoxical (REM) sleep deprivation and recovery. Eur. J. Neurosci. 21 (2005) 2488-2504
68. Verret L., Fort P., Gervasoni D., Léger L., and Luppi P.H. Localization of the neurons active during paradoxical (REM) sleep and projecting to the locus coeruleus noradrenergic neurons in the rat. J. Comp. Neurol. 495 (2006) 573-586
69. Webster H.H., and Jones B.E. Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat. II. Effects upon sleep-waking states. Brain Res. 458 (1988) 285-302
70. Wong D.L., and Tank A.W. Stress-induced catecholaminergic function: transcriptional and post-transcriptional control. Stress 10 (2007) 121-130
71. Woulfe J.M., Flumerfelt B.A., and Hrycyshyn A.W. Efferent connections of the A1 noradrenergic cell group: a DBH immunohistochemical and PHA-L anterograde tracing study. Exp. Neurol. 109 (1990) 308-322
72. Yamuy J., Mancillas J.R., Morales F.R., and Chase M.H. c-fos expression in the pons and medulla of the cat during carbachol-induced active sleep. J. Neurosci. 13 (1993) 2703-2718
73. Yamuy J., Sampogna S., Morales F.R., and Chase M.H. c-fos expression in mesopontine noradrenergic and cholinergic neurons of the cat during carbachol-induced active sleep: a double-labeling study. Sleep Res. Online 1 (1998) 28-40