Differential c-Fos immunoreactivity in arousal-promoting cell groups following systemic administration of caffeine in rats

Journal of Comparative Neurology

Volumn 498, Issue 5, 2006, Pages 667-689

  Deurveilher, Samuel ^a   Lo, Henry ^a   Murphy, Jeremy A ^a   Burns, Joan ^a   Semba, Kazue ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Aminergic; Cholinergic; Immunohistochemistry; Melanin concentrating hormone; Orexin hypocretin; Parvalbumin

Indexed keywords

CAFFEINE; MELANIN CONCENTRATING HORMONE; OREXIN; PARVALBUMIN; PROTEIN C FOS; SODIUM CHLORIDE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FOREBRAIN; IMMUNOHISTOCHEMISTRY; LOCOMOTION; LOCUS CERULEUS; MALE; NERVE CONDUCTION; NONHUMAN; NORADRENERGIC NERVE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEROTONINERGIC NERVE CELL; SUBSTANTIA NIGRA; TEGMENTUM; VENTRAL TEGMENTUM;

ANIMALS; AROUSAL; BEHAVIOR, ANIMAL; BRAIN; CAFFEINE; CELL COUNT; CENTRAL NERVOUS SYSTEM STIMULANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MOTOR ACTIVITY; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; TYROSINE 3-MONOOXYGENASE; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 33748476855     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21084     Document Type: Article

References (142)

1. Abrams JK, Johnson PL, Hay-Schmidt A, Mikkelsen JD, Shekhar A, Lowry CA. 2005. Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 133:983-997.
2. Acquas E, Tanda G, Di Chiara G. 2002. Differential effects of caffeine on dopamine and acetylcholine transmission in brain areas of drug-naive and caffeine-pretreated rats. Neuropsychopharmacology 27:182-193.
3. Alam MN, Szymusiak R, Gong H, King J, McGinty D. 1999. Adenosinergic modulation of rat basal forebrain neurons during sleep and waking: neuronal recording with microdialysis. J Physiol 521:679-690.
4. Alam MN, Kumar S, Bashir T, Suntsova N, Methippara MM, Szymusiak R, McGinty D. 2005. GABA-mediated control of hypocretin- but not melanin-concentrating hormone-immunoreactive neurones during sleep in rats. J Physiol 563:569-582.
5. 2A receptors. Psychopharmacology 183:154-162.
6. Arrigoni E, Rainnie DG, McCarley RW, Greene RW. 2001. Adenosine-mediated presynaptic modulation of glutamatergic transmission in the laterodorsal tegmentum. J Neurosci 21:1076-1085.
7. Arushanian EB, Belozertsev YB. 1978. The effect of amphetamine and caffeine on neuronal activity in the neocortex of the cat. Neuropharmacology 17:1-6.
8. Aston-Jones G, Bloom FE. 1981. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1:876-886.
9. Aston-Jones G, Cohen JD. 2005. Adaptive gain and the role of the locus coeruleus-norepinephrine system in optimal performance. J Comp Neurol 493:99-110.
10. A receptor-mediated inhibition of the nucleus accumbens shell, but not by exposure to a novel environment. Eur J Neurosci 19:376-386.
11. Basheer R, Porkka-Heiskanen T, Stenberg D, McCarley RW. 1999. Adenosine and behavioral state control: adenosine increases c-Fos protein and AP1 binding in basal forebrain of rats. Brain Res Mol Brain Res 73:1-10.
12. Bennett HJ, Semba K. 1998. Immunohistochemical localization of caffeine-induced c-Fos protein expression in the rat brain. J Comp Neurol 401:89-108.
13. Bittencourt JC, Presse F, Arias C, Peto C, Vaughan J, Nahon J-L, Vale W, Sawchenko PE. 1992. The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J Comp Neurol 319:218-245.
14. Broberger C. 1999. Hypothalamic cocaine- and amphetamine-regulated transcript (CART) neurons: histochemical relationship to thyrotropin-releasing hormone, melanin-concentrating hormone, orexin/hypocretin and neuropeptide Y. Brain Res 848:101-113.
15. Broberger C, De Lecea L, Sutcliffe JG, Hökfelt T. 1998. Hypocretin/orexin-and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J Comp Neurol 402:460-474.
16. Bubser M, Fadel JR, Jackson LL, Meador-Woodruff JH, Jing D, Deutch AY. 2005. Dopaminergic regulation of orexin neurons. Eur J Neurosci 21:2993-3001.
17. 1 receptors. J Pharmacol Exp Ther 273:637-642.
18. Cauli O, Morelli M. 2005. Caffeine and the dopaminergic system. Behav Pharmacol 16:63-77.
19. Chamberlin NL, Arrigoni E, Chou TC, Scammell TE, Greene RW, Saper CB. 2003. Effects of adenosine on GABAergic synaptic inputs to identified ventrolateral preoptic neurons. Neuroscience 119:913-918.
20. Chou DT, Forde JH, Hirsh KR. 1980. Unit activity in medial thalamus: comparative effects of caffeine and amphetamine. J Pharmacol Exp Ther 213:580-585.
21. Chou DT, Khan S, Forde J, Hirsh KR. 1985. Caffeine tolerance: behavioral, electrophysiological and neurochemical evidence. Life Sci 36:2347-2358.
22. Chu M, Huang Z-L, Qu W-M, Eguchi N, Yao M-H, Urade Y. 2004. Extracellular histamine level in the frontal cortex is positively correlated with the amount of wakefulness in rats. Neurosci Res 49:417-420.
23. Cirelli C, Pompeiano M, Tononi G. 1995. Sleep deprivation and c-fos expression in the rat brain. J Sleep Res 4:92-106.
24. 2A receptor heteromers. J Neurosci 26:2080-2087.
25. 2A agonist into the pontine reticular formation of C57BL/6J mouse increases pontine acetylcholine release and sleep. J Neurochem 96:1750-1759.
26. Cutler DJ, Morris R, Sheridhar V, Wattam TA, Holmes S, Patel S, Arch JR, Wilson S, Buckingham RE, Evans ML, Leslie RA, Williams G. 1999. Differential distribution of orexin-A and orexin-B immunoreactivity in the rat brain and spinal cord. Peptides 20:1455-1470.
27. Deurveilher S, Semba K. 2003. Indirect projections from the suprachiasmatic nucleus to the median preoptic nucleus in rat. Brain Res 987:100-106.
28. Deurveilher S, Semba K. 2006. Mapping sleep-waking control with the transcription factor c-Fos. In: Pinaud R, Tremere L, editors. Immediate early genes in sensory processing, cognitive performance and neurological disorders. Springer Scientific Press (in press).
29. Deurveilher S, Burns J, Semba K. 2002. Indirect projections from the suprachiasmatic nucleus to the median preoptic nucleus: a dual tracttracing study in rat. Sleep Suppl 25:A308.
30. Deurveilher S, Murphy JA, Burns J, Semba K. 2003. Caffeine induces c-Fos expression in arousal-related aminergic neuronal groups in rat. Sleep Suppl 26: Poster No. 77.A.
31. Deurveilher S, Lo H, Murphy JA, Burns J, Semba K. 2004. Differential activation of cholinergic and non-cholinergic neurons in the basal forebrain and mesopontine tegmentum following systemic caffeine injections in rats. Soc Neurosci Abstr Poster No. 78.6.
32. Dragunow M, Faull R. 1989. The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261-265.
33. Eriksson K, Stevens DR, Brown RE, Haas HL. 2000. Neurotransmitter actions on histaminergic neurons. In: INABIS 2000 6th Internet World Congress for Biomedical Sciences.
34. España RA, Valentino RJ, Berridge CW. 2003. Fos immunoreactivity in hypocretin-synthesizing and hypocretin-1 receptor-expressing neurons: effects of diurnal and nocturnal spontaneous waking, stress and hypocretin-1 administration. Neuroscience 121:201-217.
35. Estabrooke IV, McCarthy MT, Ko E, Chou TC, Chemelli RM, Yanagisawa M, Saper CB, Scammell TE. 2001. Fos expression in orexin neurons varies with behavioral state. J Neurosci 21:1656-1662.
36. Fadel J, Bubser M, Deutch AY. 2002. Differential activation of orexin neurons by antipsychotic drugs associated with weight gain. J Neurosci 22:6742-6746.
37. 2A and glutamate mGluR5 receptors: implications for striatal neuronal function. Proc Natl Acad Sci U S A 99:11940-11945.
38. 2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signaling. J Neurosci 17:7252-7266.
39. Fisone G, Borgkvist A, Usiello A. 2004. Caffeine as a psychomotor stimulant: mechanism of action. Cell Mol Life Sci 61:857-872.
40. Foote WE, Holmes P, Pritchard A, Hatcher C, Mordes J. 1978. Neurophysiological and pharmacodynamic studies on caffeine and on interactions between caffeine and nicotinic acid in the rat. Neuropharmacology 17:7-12.
41. Fredholm BB, Bättig K, Holmén J, Nehlig A, Zvartau EE. 1999. Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol Rev 51:83-133.
42. Freund TF. 1989. GABAergic septohippocampal neurons contain parvalbumin. Brain Res 478:375-381.
43. 1 receptor interactions in the basal ganglia. Brain Res Brain Res Rev 26:258-273.
44. 2A receptors in the ventrolateral preoptic nucleus. Neuroscience 134:1377-1390.
45. Garrett BE, Holtzman SG. 1996. Comparison of the effects of prototypical behavioral stimulants on locomotor activity and rotational behavior in rats. Pharmacol Biochem Behav 54:469-477.
46. Gasior M, Jaszyna M, Peters J, Goldberg SR. 2000. Changes in the ambulatory activity and discriminative stimulus effects of psychostimulant drugs in rats chronically exposed to caffeine: effect of caffeine dose. J Pharmacol Exp Ther 295:1101-1111.
47. Gerashchenko D, Shiromani PJ. 2004. Different neuronal phenotypes in the lateral hypothalamus and their role in sleep and wakefulness. Mol Neurobiol 29:41-59.
48. Gibbs RB, Martynowski C. 1997. Nerve growth factor induces Fos-like immunoreactivity within identified cholinergic neurons in the adult rat basal forebrain. Brain Res 753:141-151.
49. Gong H, Szymusiak R, King J, Steininger T, McGinty D. 2000. Sleep-related c-Fos protein expression in the preoptic hypothalamus: effects of ambient warming. Am J Physiol Regul Integr Comp Physiol 279: R2079-R2088.
50. Gong H, McGinty D, Guzman-Marin R, Chew KT, Stewart D, Szymusiak R. 2004. Activation of c-fos in GABAergic neurones in the preoptic area during sleep and in response to sleep deprivation. J Physiol 556:935-946.
51. Goutagny R, Luppi P-H, Salvert D, Gervasoni D, Fort P. 2005. GABAergic control of hypothalamic melanin-concentrating hormone-containing neurons across the sleep-waking cycle. Neuroreport 16:1069-1073.
52. Grant SJ, Redmond DE Jr. 1982. Methylxanthine activation of noradrenergic unit activity and reversal by clonidine. Eur J Pharmacol 85:105-109.
53. Greco MA, Lu J, Wagner D, Shiromam PJ. 2000. c-Fos expression in the cholinergic basal forebrain after enforced wakefulness and recovery sleep. Neuroreport 11:437-440.
54. Gritti I, Manns ID, Mainville L, Jones BE. 2003. Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J Comp Neurol 458:11-31.
55. Gvilia I, Turner A, McGinty D, Szymusiak R. 2006. Preoptic area neurons and the homeostatic regulation of rapid eye movement sleep. J Neurosci 26:3037-3044.
56. 2A receptors. Neuropharmacology 46:1008-1017.
57. Harris GC, Wimmer M, Aston-Jones G. 2005. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556-559.
58. Haycock JW. 1987. Stimulation-dependent phosphorylation of tyrosine hydroxylase in rat corpus striatum. Brain Res Bull 19:619-622.
59. 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 Brain Res Rev 28:370-490.
60. Hökfelt T, Johansson O, Fuxe K, Goldstein M, Park D. 1976. Immunohistochemical studies on the localization and distribution of monoamme neuron systems in the rat brain. I. Tyrosine hydroxylase in the mes-and diencephalon. Med Biol 54:427-453.
61. 1, receptors mediate the arousal effect of caffeine. Nat Neurosci 8:858-859.
62. Januǒnis S, Fite KV. 2001. Diurnal variation of c-Fos expression in subdivisions of the dorsal raphe nucleus of the Mongolian gerbil (Meriones unguiculatus). J Comp Neurol 440:31-42.
63. Johansson B, Svenningsson P, Ådén U, Lindström K, Fredholm BB. 1992. Evidence that the increase in striatal c-fos following acute high-dose caffeine is not due to direct interaction with striatal adenosine receptors. Acta Physiol Scand 146:539-541.
64. Johansson B, Lindström K, Fredholm BB. 1994. Differences in the regional and cellular localization of c-fos messenger RNA induced by amphetamine, cocaine and caffeine in the rat. Neuroscience 59:837-849.
65. Jones BE. 2005. From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26:578-586.
66. Jouvet M, Benoit O, Marsallon A, Courjon J. 1957. Action de la caféine sur l'activité électrique cérébrale [Effect of caffeine on cerebral electrical activity]. C R Séances Soc Biol Fil 151:1542-1545.
67. 2A receptors in the motor effects of caffeine after its acute and chronic administration. Neuropsychopharmacology 28:1281-1291.
68. Kiyashchenko LI, Mileykovskiy BY, Maidment N, Lam HA, Wu MF, John J, Peever J, Siegel JM. 2002. Release of hypocretin (orexin) during waking and sleep states. J Neurosci 22:5282-5286.
69. Ko EM, Estabrooke IV, McCarthy M, Scammell TE. 2003. Wake-related activity of tuberomammillary neurons in rats. Brain Res 992:220-226.
70. 2A receptor blocking agents induces caffeine-like locomotor stimulation in mice. Eur Neuropsychopharmacol 16:129-136.
71. Lee MG, Hassani OK, Jones BE. 2005. Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J Neurosci 25:6716-6720.
72. Lee RS, Steffensen SC, Henriksen SJ. 2001. Discharge profiles of ventral tegmental area GABA neurons during movement, anesthesia, and the sleep-wake cycle. J Neurosci 21:1757-1766.
73. Lena I, Parrot S, Deschaux O, Muffat-Joly S, Sauvinet V, Renaud B, Suaud-Chagny MF, Gottesmann C. 2005. Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep-wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats. J Neurosci Res 81:891-899.
74. Lin J-S, Hou Y, Jouvet M. 1996. Potential brain neuronal targets for amphetamine-, methylphenidate-, and modafinil-induced wakefulness, evidenced by c-fos immunocytochemistry in the cat. Proc Natl Acad Sci USA 93:14128-14133.
75. Lin MT, Chandra A, Liu GG. 1980. The effects of theophylline and caffeine on thermoregulatory functions of rats at different ambient temperatures. J Pharm Pharmacol 32:204-208.
76. Lu J, Chou TC, Saper CB. 2006. Identification of wake-active dopammergic neurons in the ventral periaqueductal gray matter. J Neurosci 26:193-202.
77. 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.
78. Maloney KJ, Mainville L, Jones BE. 2002. c-Fos expression in dopaminergic and GABAergic neurons of the ventral mesencephalic tegmentum after paradoxical sleep deprivation and recovery. Eur J Neurosci 15:774-778.
79. 2A adenosine receptor subtypes with a differential sensitivity to atropine. Neuroscience 116:913-920.
80. McGeorge AJ, Faull RL. 1989. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29:503-537.
81. McGinty DJ, Harper RM. 1976. Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 101:569-575.
82. 2A receptor analogs into the lateral preoptic area of rats. Am J Physiol Regul Integr Comp Physiol 289:R1715-R1723.
83. Mileykovskiy BY, Kiyashchenko LI, Siegel JM. 2005. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46:787-798.
84. 2-adrenergic receptors in basal forebrain and preoptic area express c-Fos during sleep. Neuroscience 129:803-810.
85. Modirrousta M, Mainville L, Jones BE. 2005. Orexin and MCH neurons express c-Fos differently after sleep deprivation vs. recovery and bear different adrenergic receptors. Eur J Neurosci 21:2807-2816.
86. Morairty S, Rainnie D, McCarley R, Greene R. 2004. Disinhibition of ventrolateral preoptic area sleep-active neurons by adenosine: a new mechanism for sleep promotion. Neuroscience 123:451-457.
87. Murphy JA, Deurveilher S, Semba K. 2003. Stimulant doses of caffeine induce c-Fos activation in orexin/hypocretin-containing neurons in rat. Neuroscience 121:269-275.
88. Nakajima T, Daval JL, Morgan PF, Post RM, Marangos PJ. 1989. Adenosinergic modulation of caffeine-induced c-fos mRNA expression in mouse brain. Brain Res 501:307-314.
89. Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR. 1986. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res 396:77-96.
90. Nehlig A, Boyet S. 2000. Dose-response study of caffeine effects on cerebral functional activity with a specific focus on dependence. Brain Res 858:71-77.
91. 2 receptors modulate extracellular dopamine levels in rat striatum. Neurosci Lett 212:53-56.
92. Page KJ, Saha A, Everitt BJ. 1993. Differential activation and survival of basal forebrain neurons following infusions of excitatory amino acids: studies with the immediate early gene c-fos. Exp Brain Res 93:412-422.
93. 1 receptor-activated potassium current in rat locus ceruleus neurons. J Pharmacol Exp Ther 273:537-544.
94. Panula P, Pirvola U, Auvinen S, Airaksinen MS. 1989. Histamine- immunoreactive nerve fibers in the rat brain. Neuroscience 28:585-610.
95. Paxinos G, Watson P. 1998. The rat brain in stereotaxic coordinates, 4th ed. San Diego: Academic Press.
96. Pelissier A-L, Gantenbein M, Bruguerolle B. 1999. Caffeine-induced modifications of heart rate, temperature, and motor activity circadian rhythms in rats. Physiol Behav 67:81-88.
97. Peterfi Z, Churchill L, Hajdu I, Obal F Jr, Krueger JM, Parducz A. 2004. Fos-immunoreactivity in the hypothalamus: dependency on the diurnal rhythm, sleep, gender, and estrogen. Neuroscience 124:695-707.
98. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS. 1998. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015.
99. Pickel VM, Joh TH, Reis DJ. 1976. Monoamine-synthesizing enzymes in central dopaminergic, noradrenergic and serotonergic neurons. Immunocytochemical localization by light and electron microscopy. J Histochem Cytochem 24:792-306.
100. Portas CM, Bjorvatn B, Fagerland S, Grønli J, Mundal V, Sørensen E, Ursin R. 1998. On-line detection of extracellular levels of serotonm in dorsal raphe nucleus and frontal cortex over the sleep/wake cycle in the freely moving rat. Neuroscience 83:807-814.
101. Quarta D, Borycz J, Solinas M, Patkar K, Hockemeyer J, Ciruela F, Lluis C, Franco R, Woods AS, Goldberg SR, Ferré S. 2004. Adenosine receptor-mediated modulation of dopamine release in the nucleus accumbens depends on glutamate neurotransmission and N-methyl-D-aspartate receptor stimulation. J Neurochem 91:873-880.
102. Rainnie DG, Grunze HC, McCarley RW, Greene RW. 1994. Adenosine inhibition of mesopontine cholinergic neurons: implications for EEG arousal. Science 263:689-692.
103. 1-receptors on rat locus coeruleus neurones: an intracellular electrophysiological study. Naunyn Schmiedebergs Arch Pharmacol 341:225-231.
104. Risold PY, Fellmann D, Rivier J, Vale W, Bugnon C. 1992. Immunoreactivities for antisera to three putative neuropeptides ofthe rat melanin-concentrating hormone precursor are coexpressed in neurons of the rat lateral dorsal hypothalamus. Neurosci Lett 136:145-149.
105. Sastre J-P, Buda C, Lin J-S, Jouvet M. 2000. Differential c-fos expression in the rhinencephalon and striatum after enhanced sleep-wake states in the cat. Eur J Neurosci 12:1397-1410.
106. 2 in rats. Proc Natl Acad Sci U S A 93:5980-5984.
107. 2A receptor agonist. Eur J Neurosci 11:1587-1597.
108. 2. Proc Natl Acad Sci U S A 95:7754-7759.
109. Scammell TE, Estabrooke IV, McCarthy MT, Chemelli RM, Yanagisawa M, Miller MS, Saper CB. 2000. Hypothalamic arousal regions are activated during modafinil-induced wakefulness. J Neurosci 20:8620-8628.
110. Schwierin B, Borbély AA, Tobler I. 1996. Effects of N6-cyclopentyl-adenosine and caffeine on sleep regulation in the rat. Eur J Pharmacol 300:163-171.
111. Semba K. 1999. The mesopontine cholinergic system: a dual role in REM sleep and wakefulness. In: Lydic R, Baghdoyan H, editors. Handbook of behavioral state control. Cellular and molecular mechanisms. Boca Raton, FL: CRC Press, p 161-180.
112. Semba K. 2000. Multiple output pathways of the basal forebrain: organization, chemical heterogeneity, and roles in vigilance. Behav Brain Res 115:117-141.
113. Sherin J, Shiromani P, McCarley R, Saper C. 1996. Activation of ventro-lateral preoptic neurons during sleep. Science 271:216-219.
114. Shouse MN, Staba RJ, Saquib SF, Farber PR. 2000. Monoamines and sleep: microdialysis findings in pons and amygdala. Brain Res 860:181-189.
115. Singewald N, Sharp T. 2000. Neuroanatomical targets of anxiogenic drugs in the hindbrain as revealed by Fos immunocytochemistry. Neuroscience 98:759-770.
116. Singewald N, Salchner P, Sharp T. 2003. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol Psychiatry 53:275-283.
117. Sloviter RS. 1989. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183-196.
118. Solinas M, Ferré S, You Z-B, Karcz-Kubicha M, Popoli P, Goldberg SR. 2002. Caffeine induces dopamine and glutamate release in the shell of the nucleus accumbens. J Neurosci 22:6321-6324.
119. Steinbusch HW. 1981. Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557-618.
120. Steinfels GF, Heym J, Jacobs BL. 1981. Single unit activity of dopaminergic neurons in freely moving cats. Life Sci 29:1435-1442.
121. Stoner GR, Skirboll LR, Werkman S, Hommer DW. 1988. Preferential effects of caffeine on limbic and cortical dopamine systems. Biol Psychiatry 23:761-768.
122. Strecker RE, Nalwalk J, Dauphin LJ, Thakkar MM, Chen Y, Ramesh V, Hough LB, McCarley RW. 2002. Extracellular histamine levels in the feline preoptic/anterior hypothalamic area during natural sleep-wakefulness and prolonged wakefulness: an in vivo microdialysis study. Neuroscience 113:663-670.
123. Svenningsson P, Johansson B, Fredholm BB. 1995a. Effect of different xanthines and phosphodiesterase inhibitors on c-fos expression in rat striatum. Acta Physiol Scand 154:17-24.
124. Svenningsson P, Nomikos GG, Fredholm BB. 1995b. Biphasic changes in locomotor behavior and in expression of mRNA for NGFI-A and NGFI-B in rat striatum following acute caffeine administration. J Neurosci 15:7612-7624.
125. Svenningsson P, Strom A, Johansson B, Fredholm BB. 1995c. Increased expression of c-jun, junB, AP-1, and preproenkephalin mRNA in rat striatum following a single injection of caffeine. J Neurosci 15:3583-3593.
126. Taguchi Y, Watanabe T, Kubota H, Hayashi H, Wada H. 1984. Purification of histidine decarboxylase from the liver of fetal rats and its immunochemical and immunohistochemical characterization. J Biol Chem 259:5214-5221.
127. Thakkar MM, Delgiacco RA, Strecker RE, McCarley RW. 2003. Adenosinergic inhibition of basal forebrain wakefulness-active neurons: a simultaneous unit recording and microdialysis study in freely behaving cats. Neuroscience 122:1107-1113.
128. Tononi G, Pompeiano M, Cirelli C. 1994. The locus coeruleus and immediate-early genes in spontaneous and forced wakefulness. Brain Res Bull 35:589-596.
129. Torterolo P, Yamuy J, Sampogna S, Morales FR, Chase MH. 2001. GABAergic neurons of the laterodorsal and pedunculopontine tegmental nuclei of the cat express c-fos during carbachol-induced active sleep. Brain Res 892:309-319.
130. Torterolo P, Yamuy J, Sampogna S, Morales FR, Chase MH. 2003. Hypocretinergic neurons are primarily involved in activation of the somatomotor system. Sleep 26:25-28.
131. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK. 1994. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J Comp Neurol 348:351-373.
132. Valdés JL, Farías P, Ocampo-Garcés A, Cortés N, Serón-Ferré M, Torrealba F. 2005. Arousal and differential Fos expression in histaminergic neurons of the ascending arousal system during a feeding-related motivated behaviour. Eur J Neurosci 21:1931-1942.
133. Vanni-Mercier G, Gigout S, Debilly G, Lin J-S. 2003. Waking selective neurons in the posterior hypothalamus and their response to histamine H3-receptor ligands: an electrophysiological study in freely moving cats. Behav Brain Res 144:227-241.
134. Verret L, Goutagny R, Fort P, Cagnon L, Salvert D, Léger L, Boissard R, Salin P, Peyron C, Luppi P-H. 2003. A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neurosci 4:19.
135. Verret L, Léger L, Fort P, Luppi P-H. 2005. Cholinergic and noncholinergic brainstem neurons expressing Fos after paradoxical (REM) sleep deprivation and recovery. Eur J Neurosci 21:2488-2504.
136. Wager-Srdar SA, Oken MM, Morley JE, Levine AS. 1983. Thermoregulatory effects of purines and caffeine. Life Sci 33:2431-2438.
137. Watanabe T, Taguchi Y, Shiosaka S, Tanaka J, Kubota H, Terano Y, Tohyama M, Wada H. 1984. Distribution of the histaminergic neuron system in the central nervous system of rats: a fluorescent immunohistochemical analysis with histidine decarboxylase as a marker. Brain Res 295:13-25.
138. Wise RA. 2005. Forebrain substrates of reward and motivation. J Comp Neurol 493:115-121.
139. Yamuy J, Sampogna S, López-Rodríguez F, Luppi P-H, Morales FR, Chase MH. 1995. Fos and serotonin immunoreactivity in the raphe nuclei of the cat during carbachol-induced active sleep: a double-labeling study. Neuroscience 67:211-223.
140. Yamuy J, Sampogna S, Morales FR, Chase MH. 1998. c-fos expression in mesopontine noradrenergic and cholinergic neurons of the cat during carbachol-induced active sleep: a double-labeling study. Sleep Res Online 1:28-40.
141. Yanik G, Glaum S, Radulovacki M. 1987. The dose-response effects of caffeine on sleep in rats. Brain Res 403:177-180.
142. Zar JH. 1999. Biostatistical analysis. Englewood Cliffs, NJ: Prentice Hall.