Genetic deletion of fatty acid amide hydrolase alters emotional behavior and serotonergic transmission in the dorsal raphe, prefrontal cortex, and hippocampus

Neuropsychopharmacology

Volumn 35, Issue 10, 2010, Pages 2083-2100

  Bambico, Francis Rodriguez ^a   Cassano, Tommaso ^b   Dominguez Lopez, Sergio ^a   Katz, Noam ^a   Walker, Claire Dominique ^c   Piomelli, Daniele ^d   Gobbi, Gabriella ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF FOGGIA   (Italy)

^c DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cannabinoid CB1 receptor; depression anxiety; electrophysiology; fatty acid amide hydrolase (FAAH) knockout; rimonabant; serotonin

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; ANTIDEPRESSANT AGENT; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; FATTY ACID AMIDASE; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; RIMONABANT; SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN 2A AGONIST; SEROTONIN 2A RECEPTOR; SEROTONIN 2C AGONIST; SEROTONIN 2C RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; DRUG ACTIVITY; ELECTROPHYSIOLOGY; EMOTION; FEEDING; FORCED SWIMMING TEST; GENE DELETION; HIPPOCAMPUS; IMMOBILIZATION; MALE; MAZE TEST; MOUSE; NONHUMAN; PHENOTYPE; PREFRONTAL CORTEX; PRIORITY JOURNAL; REARING; TRANQUILIZING ACTIVITY; WILD TYPE;

ACTION POTENTIALS; AMIDOHYDROLASES; ANIMALS; BEHAVIOR, ANIMAL; BENZAMIDES; BRAIN; CARBAMATES; ENZYME INHIBITORS; EXPLORATORY BEHAVIOR; HINDLIMB SUSPENSION; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOOD DISORDERS; PIPERIDINES; PREFRONTAL CORTEX; PYRAZOLES; RAPHE NUCLEI; RECEPTORS, CANNABINOID; SEROTONIN; SEROTONIN AGENTS; SWIMMING;

EID: 77955716188     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2010.80     Document Type: Article

References (105)

1. Adamec R, Creamer K, Bartoszyk GD, Burton P (2004). Prophylactic and therapeutic effects of acute systemic injections of EMD 281014, a selective serotonin 2A receptor antagonist on anxiety induced by predator stress in rats. Eur J Pharmacol 504: 79-96.
2. Aghajanian GK, Wang RY, Baraban J (1978). Serotonergic and non-serotonergic neurons of dorsal rapheFreciprocal changes in firing induced by peripheral-nerve stimulation. Brain Res 153: 169-175.
3. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B et al (2005). The endocannabinoid system drives neural progenitor proliferation. FASEB J 19: 1704-1706.
4. Aguado T, Palazuelos J, Monory K, Stella N, Cravatt B, Lutz B et al (2006). The endocannabinoid system promotes astroglial differ-entiation by acting on neural progenitor cells. J Neurosci 26: 1551-1561.
5. Allers KA, Sharp T (2003). Neurochemical and anatomical identification of fast-and slow-firing neurones in the rat dorsal raphe nucleus using juxtacellular labelling methods in vivo. Neuroscience 122: 193-204.
6. Archer J (1973). Tests for emotionality in rats and miceFreview. Anim Behav 21: 205-235.
7. Ashby CR, Jiang LH, Kasser RJ, Wang RY (1990). Electrophysio-logical characterization of 5-hydroxytryptamine-2 receptors in the rat medial prefrontal cortex. J Pharmacol Exp Ther 252: 171-178.
8. Aso E, Renoir T, Mengod G, Ledent C, Hamon M, Maldonado R et al (2009). Lack of CB1 receptor activity impairs serotonergic negative feedback. J Neurochem 109: 935-944.
9. Bambico FR, Duranti A, Tontini A, Tarzia G, Gobbi G (2009a). Endocannabinoids in the treatment of mood disorders: evidence from animal models. Curr Pharm Des 15: 1623-1646.
10. Bambico FR, Gobbi G (2008). The cannabinoid CB1 receptor and the endocannabinoid anandamide: possible antidepressant targets. Expert Opin Ther Targets 12: 1347-1366.
11. Bambico FR, Katz N, Debonnel G, Gobbi G (2007). Cannabinoids elicit antidepressant-like behavior and activate serotonergic neurons through the medial prefrontal cortex. J Neurosci 27: 11700-11711.
12. Bambico FR, Nguyen NT, Gobbi G (2009b). Decline in serotonergic firing activity and desensitization of 5-HT1A autoreceptors after chronic unpredictable stress. Eur Neuropsychopharmacol 19: 215-228.
13. Bambico FR, Nguyen NT, Katz N, Gobbi G (2010). Chronic exposure to cannabinoids during adolescence but not during adulthood impairs emotional behaviour and monoaminergic neurotransmission. Neurobiol Dis 37: 641-655.
14. Baraban JM, Aghajanian GK (1980). Suppression of serotonergic neuronal firing by alpha-adrenoceptor antagonistsFevidence against GAHA mediation. Eur J Pharmacol 66: 287-294.
15. Bartho P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsaki G (2004). Characterization of neocortical principal cells and Interneurons by network interactions and extracellular features. J Neurophysiol 92: 600-608.
16. Basavarajappa BS, Yalamanchili R, Cravatt BF, Cooper TB, Hungund BL (2006). Increased ethanol consumption and preference and decreased ethanol sensitivity in female FAAH knockout mice. Neuropharmacology 50: 834-844.
17. Besson A, Haddjeri N, Blier P, de Montigny C (2000). Effects of the co-administration of mirtazapine and paroxetine on serotoner-gic neurotransmission in the rat brain. Eur Neuropsychophar-macol 10: 177-188.
18. Blokland A, Lieben C, Deutz NEP (2002). Anxiogenic and depressive-like effects, but no cognitive deficits, after repeated moderate tryptophan depletion in the rat. J Psychopharmacol 16: 39-49.
19. Bodnoff SR, Suranyicadotte B, Aitken DH, Quirion R, Meaney MJ (1988). The effects of chronic antidepressant treatment in an animal-model of anxiety. Psychopharmacology 95: 298-302.
20. Bortolato M, Mangieri RA, Fu J, Kim JH, Arguello O, Duranti A et al (2007). Antidepressant-like activity of the fatty acid amide hydrolase inhibitor URB597 in a rat model of chronic mild stress. Biol Psychiatry 62: 1103-1110.
21. Celada P, Puig MV, Casanovas JM, Guillazo G, Artigas F (2001). Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: involvement of serotonin-1A, GABA(A), and glutamate receptors. J Neurosci 21: 9917-9929.
22. Cheer JF, Cadogan AK, Marsden CA, Fone KCF, Kendall DA (1999). Modification of 5-HT2 receptor mediated behaviour in the rat by oleamide and the role of cannabinoid receptors. Neuropharmacology 38: 533-541.
23. Choleris E, Thomas AW, Kavaliers M, Prato FS (2001). A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci Biobehav Rev 25: 235-260.
24. Cole JC, Rodgers RJ (1995). Ethological comparison of the effects of diazepam and acute chronic imipramine on the behavior of mice in the elevated plus-maze. Pharmacol Biochem Behav 52: 473-478.
25. Conductier G, Dusticier N, Lucas G, Cote F, Debonnel G, Daszuta A et al (2006). Adaptive changes in serotonin neurons of the raphe nuclei in 5-HT4 receptor knock-out mouse. Eur J Neurosci 24: 1053-1062.
26. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR et al (2001). Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci USA 98: 9371-9376.
27. Dahlstrom A, Fuxe K (1964). Evidence for existence of mono-amine-containing neurons in central nervous system. I. Demonstration of monoamines in cell bodies of brain stem neurons. Acta Physiol Scand 232(Suppl): 1-55.
28. Deakin JFW (1988). 5HT2 receptors, depression and anxiety. Pharmacol Biochem Behav 29: 819-820.
29. Descarries L, Watkins KC, Garcia S, Beaudet A (1982). The serotonin neurons in nucleus raphe dorsalis of adult-ratFa light and electron-microscope autoradiographic study. J Comp Neurol 207: 239-254.
30. Dorr AE, Debonnel G (2006). Effect of vagus nerve stimulation on serotonergic and noradrenergic transmission. J Pharmacol Exp Ther 318: 890-898.
31. Egertova M, Giang DK, Cravatt BF, Elphick MR (1998). A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc Roy Soc Lon B-Biol Sci 265: 2081-2085.
32. ElMansari M, Blier P (1997). In vivo electrophysiological characterization of 5-HT receptors in the guinea pig head of caudate nucleus and orbitofrontal cortex. Neuropharmacology 36: 577-588.
33. Germine M, Goddard AW, Sholomskas DE, Woods SW, Charney DS, Heninger GR (1994). Response to meta-chlorophenylpiper-azine in panic disorder patients and healthy-subjectsFinfluence of reduction in intravenous dosage. Psychiatry Res 54: 115-133.
34. Gobbi G, Bambico FR, Mangieri R, Bortolato M, Campolongo P, Solinas M et al (2005). Antidepressant-like activity and modulation of brain monoaminergic transmission by blockade of anandamide hydrolysis. Proc Natl Acad Sci USA 102: 18620-18625.
35. Gobbi G, Janiri L (2006). Sodium-and magnesium-valproate in vivo modulate glutamatergic and GABAergic synapses in the medial prefrontal cortex. Psychopharmacology 185: 255-262.
36. Gobbi G, Murphy DL, Lesch KP, Blier P (2001). Modifications of the serotonergic system in mice lacking serotonin transporters: an in vivo electrophysiological study. J Pharmacol Exp Ther 296: 987-995.
37. Griebel G, Rodgers RJ, Perrault G, Sanger DJ (1997). Risk assessment behaviour: evaluation of utility in the study of 5-HT-related drugs in the rat elevated plus-maze test. Pharmacol Biochem Behav 57: 817-827.
38. Gross C, Santarelli L, Brunner D, Zhuang XX, Hen R (2000). Altered fear circuits in 5-HT1A receptor KO mice. Biol Psychiatry 48: 1157-1163.
39. Haddjeri N, Blier P (2001). Sustained blockade of neurokinin-1 receptors enhances serotonin neurotransmission. Biol Psychiatry 50: 191-199.
40. Haddjeri N, Blier P, de Montigny C (1998). Long-term antide-pressant treatments result in a tonic activation of forebrain 5-HT1A receptors. J Neurosci 18: 10150-10156.
41. Haddjeri N, Blier P, deMontigny C (1996). Effect of the alpha-2 adrenoceptor antagonist mirtazapine on the 5-hydroxytrypta-mine system in the rat brain. J Pharmacol Exp Ther 277: 861-871.
42. Haj-Dahmane S, Shen RY (2009). Endocannabinoids suppress excitatory synaptic transmission to Dorsal Raphe serotonin neurons through the activation of presynaptic CB1 receptors. J Pharmacol Exp Ther 331: 186-196.
43. Haller J, Barna I, Barsvari B, Pelczer KG, Yasar S, Panlilio LV et al (2009). Interactions between environmental aversiveness and the anxiolytic effects of enhanced cannabinoid signaling by FAAH inhibition in rats. Psychopharmacology 204: 607-616.
44. Haring M, Marsicano G, Lutz B, Monory K (2007). Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice. Neuroscience 146: 1212-1219.
45. Heurteaux C, Lucas G, Guy N, El Yacoubi M, Thummler S, Peng XD et al (2006). Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nat Neurosci 9: 1134-1141.
46. Hill MN, Gorzalka BB (2005). Pharmacological enhancement of cannabinoid CB1 receptor activity elicits an antidepressant-like response in the rat forced swim test. Eur Neuropsychopharmacol 15: 593-599.
47. Hill MN, Hillard CJ, Bambico FR, Patel S, Gorzalka BB, Gobbi G (2009a). The therapeutic potential of the endocannabinoid system for the development of a novel class of antidepressants. Trends in Pharmacol Sci 30: 484-493.
48. Hill MN, McEwen BS (2009). Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorti-coids. Prog Neuropsychopharmacol Biol Psychiatry (E-pub ahead of print 10 November 2009).
49. Hill MN, McLaughlin RJ, Morrish AC, Viau V, Floresco SB, Hillard CJ et al (2009b). Suppression of amygdalar endocan-nabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology 34: 2733-2745.
50. Hill MN, Sun JC, Tse MTL, Gorzalka BB (2006). Altered responsiveness of serotonin receptor subtypes following long-term cannabi-noid treatment. Int J Neuropsychopharmacol 9: 277-286.
51. Hogg S (1996). A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Bioch Behav 54: 21-30.
52. Hollander E, Decaria C, Gully R, Nitescu A, Suckow RF, Gorman JM et al (1991a). Effects of chronic fluoxetine treatment on behavioral and neuroendocrine responses to meta-chlorophe-nylpiperazine in obsessive-compulsive disorder. Psychiatry Res 36: 1-17.
53. Hollander E, Decaria C, Gully R, Nitescu A, Suckow RF, Gorman JM et al (1991b). Effects of chronic fluoxetine treatment on behavioral and neuroendocrine responses to meta-chlorophe-nylpiperazine in obsessive-compulsive disorder. Psychiatry Res 36: 1-17.
54. Holmes A (2008). Genetic variation in cortico-amygdala serotonin function and risk for stress-related disease. Neurosci Biobehav Rev 32: 1293-1314.
55. Holtzman D, Lovell RA, Jaffe JH, Freedman DX (1969). 1-delta9- tetrahydrocannabinolFneurochemical and behavioral effects in mouse. Science 163: 1464-1467.
56. Jacobs BL, van Praag H, Gage FH (2000). Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatry 5: 262-269.
57. Johnson KM, Dewey WL, Harris LS (1976). Delta-9-ThC induced elevations of mouse-brain tryptophan and consequent increased serotonin production. Pharmacologist 18: 166.
58. Kandel ER, Spencer WA (1961). Electrophysiological properties of an archicortical neuron. Ann NY Acad Sci 94: 570-603.
59. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A et al (2003). Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9: 76-81.
60. Kelliher P, Connor TJ, Harkin A, Sanchez C, Kelly JP, Leonard BE (2000). Varying responses to the rat forced-swim test under diurnal and nocturnal conditions. Physiol Behav 69: 531-539.
61. Kennett GA, Lightowler S, Debiasi V, Stevens NC, Wood MD, Tulloch IF et al (1994a). Effect of chronic administration of selective 5-hydroxytryptamine and noradrenaline uptake inhibitors on a putative index of 5-HT2C/2B receptor function. Neuropharmacology 33: 1581-1588.
62. Kennett GA, Lightowler S, Murphy O, Debiasi V, Stevens N, Tulloch LF et al (1994b). Chronic treatment with paroxetine and fluoxetine, but not desipramine, desensitizes 5-HT2C receptor function. Br J Pharmacol 112: U109.
63. Kennett GA, Pittaway K, Blackburn TP (1994c). Evidence that 5-HT2C receptor antagonists are anxiolytic in the rat Geller-Seifter model of anxiety. Psychopharmacology 114: 90-96.
64. Kinney GG, Vogel GW, Feng PF (1997). Decreased dorsal raphe nucleus neuronal activity in adult chloral hydrate anesthetized rats following neonatal clomipramine treatment: Implications for endogenous depression. Brain Res 756: 68-75.
65. Labonte B, Bambico FR, Gobbi G (2009). Potentiation of excitatory serotonergic responses by MK-801 in the medial prefrontal cortex. Naunyn-Schmiedebergs Arch Pharmacol 380: 383-397.
66. Linner L, Wiker C, Arborelius L, Schalling M, Svensson TH (2004). Selective noradrenaline reuptake inhibition enhances serotoner-gic neuronal activity and transmitter release in the rat forebrain. J Neural Transm 111: 127-139.
67. Maes M, Meltzer HY (1995). The serotonin hypothesis of major depression. In: Bloom F, Kupfer D (eds). Psychopharmacology: the fourth generation of progress. Raven Press: New York. pp 933-944.
68. Marek GJ, Carpenter LL, McDougle CJ, Price H (2003). Synergistic action of 5-HT2A antagonists and selective serotonin reuptake inhibitors in neuropsychiatric disorders. Neuropsychoparmaco-logy 28: 402-412.
69. Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O (2002). Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology 159: 379-387.
70. Miczek KA, Dixit BN (1980). Behavioral and biochemical effects of chronic delta-9-tetrahydrocannabinol in rats. Psychopharmacol-ogy 67: 195-202.
71. 2-induced anxiety in patients with panic disorder and normal volunteers. Br J Psychiatry 176: 182-188.
72. Moldrich G, Wenger T (2000). Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides 21: 1735-1742.
73. Moranta D, Esteban S, Garcia-Sevilla JA (2004). Differential effects of acute cannabinoid drug treatment, mediated by CB1 receptors, on the in vivo activity of tyrosine and tryptophan hydroxylase in the rat brain. Naunyn-Schmiedebergs Arch Pharmacol 369: 516-524.
74. Moreira FA, Kaiser N, Monory K, Lutz B (2008). Reduced anxietylike behaviour induced by genetic and pharmacological inhibition of the endocannabinoid-degrading enzyme fatty acid amide hydrolase (FAAH) is mediated by CB1 receptors. Neuropharma-cology 54: 141-150.
75. Naidu PS, Varvel SA, Ahn K, Cravatt BF, Martin BR, Lichtman AH (2007). Evaluation of fatty acid amide hydrolase inhibition in murine models of emotionality. Psychopharmacology 192: 61-70.
76. Navarro M, Hernandez E, Munoz RM, delArco I, Villanua MA, Carrera MRA et al (1997). Acute administration of the CB1 cannabinoid receptor antagonist SR141716A induces anxietylike responses in the rat. Neuroreport 8: 491-496.
77. Ohayon MM (2006). Anxiety disorders: prevalence, comorbidity and outcomes. J Psychiatric Res 40: 475-476.
78. Patel S, Hillard CJ (2006). Pharmacological evaluation of cannabinoid receptor ligands in a mouse model of anxiety: further evidence for an anxiolytic role for endogenous canna-binoid signaling. J Pharmacol Exp Ther 318: 304-311.
79. Patel S, Roelke CT, Rademacher DJ, Hillard CJ (2005). Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur J Neurosci 21: 1057-1069.
80. Paxinos G, Franklin KBJ (2001). The Mouse Brain in Stereotaxic Coordinates (Ed 2). Academic: London.
81. Pellow S, File SE (1986). Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-mazeFa novel test of anxiety in the rat. Pharmacol Biochem Beh 24: 525-529.
82. Pineyro G, Blier P, Dennis T, deMontigny C (1994). Desensitization of the neuronal 5-HT carrier following its long-term blockade. J Neurosci 14: 3036-3047.
83. Pistis M, Muntoni AL, Gessa G, Diana M (1997). Effects of acute, chronic ethanol and withdrawal on dorsal raphe neurons: electrophysiological studies. Neuroscience 79: 171-176.
84. Porsolt RD, Lepichon M, Jalfre M (1977). Depression Fnew animal-model sensitive to antidepressant treatments. Nature 266: 730-732.
85. Quested DJ, Sargent PA, Cowen PJ (1997). SSRI treatment decreases prolactin and hyperthermic responses to mCPP. Psychopharmacology 133: 305-308.
86. Rago L, Kiivet RA, Harro J, Pold M (1988). Behavioral-differences in an elevated plus-mazeFcorrelation between anxiety and decreased number of GABA and benzodiazepine receptors in mouse cerebral-cortex. Naunyn-Schmiedebergs Arch Pharmacol 337: 675-678.
87. Rodgers RJ, Cole JC, Aboualfa K, Stephenson LH (1995). Ethopharmacological analysis of the effects of putative anxio-genic agents in the mouse elevated plus-maze. Pharmacol Biochem Behav 52: 805-813.
88. Roiser JP, Levy J, Fromm SJ, Wang HY, Hasler G, Sahakian BJ et al (2008). The effect of acute tryptophan depletion on the neural correlates of emotional processing in healthy volunteers. Neuropsychopharmacology 33: 1992-2006.
89. Sagredo O, Ramos JA, Fernandez-Ruiz J, Rodriguez M, de Miguel R (2006). Chronic delta(9)-tetrahydrocannabinol administration affects serotonin levels in the rat frontal cortex. Naunyn-Schmiedebergs Arch Pharmacol 372: 313-317.
90. Santarelli L, Gobbi G, Debs PC, Sibille EL, Blier P, Hen R et al (2001). Genetic and pharmacological disruption of neurokinin 1 receptor function decreases anxiety-related behaviors and increases sero-tonergi function. Proc Natl Acad Sci USAm 98: 1912-1917.
91. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805-809.
92. Smith KA, Fairburn CG, Cowen PJ (1997). Relapse of depression after rapid depletion of tryptophan. Lancet 349: 915-919.
93. Steinbusch HWM (1981). Distribution of serotonin-immunoreac-tivity in the central nervous-system of the ratFcell-bodies and terminals. Neuroscience 6: 557-618.
94. Steru L, Chermat R, Thierry B, Simon P (1985). The tail suspension testFa new method for screening antidepressants in mice. Psychopharmacology 85: 367-370.
95. Szabo ST, Blier P (2001a). Effect of the selective noradrenergic reuptake inhibitor reboxetine on the firing activity of noradrena-line and serotonin neurons. E J Neurosci 13: 2077-2087.
96. Szabo ST, Blier P (2001b). Effects of the selective norepinephrine reuptake inhibitor reboxetine on norepinephrine and serotonin transmission in the rat hippocampus. Neuropsychopharmacology 25: 845-857.
97. Temel Y, Boothman LJ, Blokland A, Magill PJ, Steinbusch HWM, Visser-Vandewalle V et al (2007). Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci USA 104: 17087-17092.
98. Urbain N, Creamer K, Debonnel G (2006). Electrophysiological diversity of the dorsal raphe cells across the sleep-wake cycle of the rat. J Physiol London 573: 679-695.
99. Uriguen L, Perez-Rial S, Ledent C, Palomo T, Manzanares J (2004). Impaired action of anxiolytic drugs in mice deficient in cannabinoid CB1 receptors. Neuropharmacology 46: 966-973.
100. Vandermaelen CP, Aghajanian GK (1983). Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat-brain slices. Brain Res 289: 109-119.
101. Vaswani M, Linda FK, Ramesh S (2003). Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review. Prog Neuro-Psychopharmacol Biol Psychiatry 27: 85-102.
102. Walf AA, Frye CA (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protocols 2: 322-328.
103. Zahorodna A, Hess G (2006). Imipramine and citalopram reverse corticosterone-induced alterations in the effects of the activation of 5-HT1A and 5-HT2 receptors in rat frontal cortex. J Physiol Pharmacol 57: 389-399.
104. Zhou JS, Li LJ, Tang SJ, Cao X, Li ZX, Li WH et al (2008). Effects of serotonin depletion on the hippocampal GR/MR and BDNF expression during the stress adaptation. Behav Brain Res 195: 129-138.
105. Zisook S, Ganadjian K, Moutier C, Prather R, Rao S (2008). Sequenced treatment alternatives to relieve depression (STAR*D): lessons learned. J Clin Psychiatry 69: 1184-1185.