Serotonin and emotion, learning and memory

Reviews in the Neurosciences

Volumn 23, Issue 5-6, 2012, Pages 543-553

  Meneses, Alfredo ^a   Liy Salmeron, Gustavo ^b  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD ANÁHUAC   (Mexico)

Author keywords

Emotion; Memory; Serotonin

Indexed keywords

AZASETRON; BUSPIRONE; FLUOXETINE; FLUVOXAMINE; GEPIRONE; GRANISETRON; NARATRIPTAN; OLANZAPINE; ONDANSETRON; PAROXETINE; QUETIAPINE; RISPERIDONE; SEROTONIN 1 RECEPTOR; SEROTONIN 1A AGONIST; SEROTONIN 2 RECEPTOR; SEROTONIN 2A AGONIST; SEROTONIN 4 AGONIST; SEROTONIN 6 ANTAGONIST; SEROTONIN 7 RECEPTOR; SEROTONIN RECEPTOR; SEROTONIN TRANSPORTER; SUMATRIPTAN; TANDOSPIRONE; ZOLMITRIPTAN;

ARTICLE; EMOTION; HUMAN; LEARNING; MEMORY; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; EMOTIONS; HUMANS; LEARNING; SEROTONIN; SEROTONIN AGENTS; SIGNAL TRANSDUCTION;

EID: 84869422392     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/revneuro-2012-0060     Document Type: Article

References (103)

1. Aboukhatwa, M., Dosanjh, L., and Luo, Y. (2010). Antidepressants are a rational complementary therapy for the treatment of Alzheimer's disease. Mol. Neurodegener. 5, 10.
2. Aloyo, V.J., Berg, K.A., Spampinato, U., Clarke, W.P., and Harvey, J.A. (2009). Current status of inverse agonism at serotonin 2A (5-HT 2A) and 5-HT 2C receptors. Pharmacol. Ther. 121, 160-173.
3. Barnes, N.M. and Sharp, T. (1999). A review of central 5-HT receptors and their function. Neuropharmacology 38, 1083-1152.
4. Baudry, A., Mouillet-Richard, S., Schneider, B., Launay, J.M., and Kellermann, O. (2010). miR-16 targets the serotonin transporter: a new facet for adaptive responses to antidepressants. Science 329, 1537-1541.
5. Bienfang, D.C., McKenna, M.J., Papaliodis, G.N., Gonzalez, R.G., and Stemmer-Rachamimov, A. (2011). Case records of the Massachusetts General Hospital. Case 24-2011. A 36-year-old man with headache, memory loss, and confusion. N. Engl. J. Med. 365, 549-559.
6. Birmes, P., Senard, J.M., Escande, M., and Schmitt, L. (2002). Biological factors of PTSD: neurotransmitters and neuromodulators. Encephale 28, 241-247.
7. Bockaert, J., Claeysen, S., Compan, V., and Dumuis, A. (2008). 5-HT (4) receptors: history, molecular pharmacology and brain functions. Neuropharmacology 55, 922-931.
8. Bohn, L.M. and Schmid, C.L. (2010). Serotonin receptor signaling and regulation via β -arrestins. Crit. Rev. Biochem. Mol. Biol. 45, 555-566.
9. Bonsi, P., Cuomo, D., Ding, J., Sciamanna, G., Ulrich, S., Tscherter, A., Bernardi, G., Surmeier, D.J., and Pisani, A. (2007). Endogenous serotonin excites striatal cholinergic interneurons via the activation of 5-HT 2C, 5-HT 6, and 5-HT 7 serotonin receptors: implications for extrapyramidal side effects of serotonin reuptake inhibitors. Neuropsychopharmacology 32, 1840-1854.
10. Borroni, B., Costanzi, C., and Padovani, A. Genetic susceptibility to behavioural and psychological symptoms in Alzheimer disease. Curr. Alzheimer Res. 7, 158-164.
11. Buhot, M.C., Wolff, M., and Segu, L. (2003). Serotonin. In: Memories Are Made of These: From Messengers to Molecules. G. Riedel and B. Platt, eds. (Kluwer Academic/Plenum Publishers), pp. 1-19.
12. Cassel, J.C. (2010). Experimental Studies on the Role(s) of Serotonin in Learning and Memory Functions. In: Handbook of the Behavioral Neurobiology of Serotonin, Vol. 21. C.P. Müller and B.L. Jacobs, eds. (Amsterdam: Academic Press), pp. 429-447.
13. Cassel, J.C. and Jeltsch, H. (1995). Serotonergic modulation of cholinergic function in the central nervous system: cognitive implications. Neuroscience 69, 1-41.
14. Cerejeira, J., Lagarto, L., and Mukaetova-Ladinska, E.B. (2012). Behavioral and psychological symptoms of dementia. Front. Neurol. 3, 73.
15. Chamberlain, S.R., Müller, U., Robbins, T.W., and Sahakian, B.J. (2006). Neuropharmacological modulation of cognition. Curr. Opin. Neurol. 19, 607-612.
16. de Almeida, J., Palacios, J.M., and Mengod, G. (2008). Distribution of 5-HT and DA receptors in primate prefrontal cortex: implications for pathophysiology and treatment. Prog. Brain Res. 172, 101-115.
17. Eriksson, T.M., Delagrange, P., Spedding, M., Popoli M., Math e, A.A., O gren, S.O., and Svenningsson, P. (2012a). Emotional memory impairments in a genetic rat model of depression: involvement of 5-HT/MEK/Arc signaling in restoration. Mol. Psychiatry 17, 173-184.
18. Eriksson, T.M., Holst, S., Stan, T.L., Hager, T., Sjogren, B., Ogren, S.O., Svenningsson, P., and Stiedl, O. (2012b). 5-HT 1A and 5-HT 7 receptor crosstalk in the regulation of emotional memory: implications for effects of selective serotonin reuptake inhibitors. Neuropharmacology 63, 1150-1160.
19. Eriksson, T.M., Delagrange, P., Spedding, M., Popoli, M., Mathe, A.A., Ogren, S.O., and Svenningsson, P. (2012c). http://www.ncbi.nlm.nih.gov/pubmed/ 21242991. Emotional memory impairments in a genetic rat model of depression: involvement of 5-HT/MEK/Arc signaling in restoration. Mol. Psychiatry 17, 173-184.
20. Ersche, K.D., Roiser, J.P., Lucas, M., Domenici, E., Robbins, T.W., and Bullmore, E.T. (2011). Peripheral biomarkers of cognitive response to dopamine receptor agonist treatment. Psychopharmacology (Berl) 214, 779-789.
21. Evers, E.A.T., Tillie, D.E., van der Veen, F.M., Lieben, C.K., Jolles, J., Deutz, N.E.P., and Schmitt, J.A.J. (2005). Effects of a novel method of acute tryptophan depletion on plasma tryptophan and cognitive performance in healthy volunteers. Psychopharmacology (Berl) 178, 92-99.
22. Fusar-Poli, P., Allen, P., McGuire, P., Placentino, A., Cortesi, M., and Perez, J. (2006). Neuroimaging and electrophysiological studies of the effects of acute tryptophan depletion: a systematic review of the literature. Psychopharmacology (Berl) 188, 131-143.
23. Garner, A.R., Rowland, D.C., Hwang, S.Y., Baumgarten, K., Roth, B.L., Kentros, C., and Mayford M. (2012). Generation of a synthetic memory trace. Science 335, 1513-1516.
24. Greenwood, B.N. and Fleshner, M. (2011). Exercise, stress resistance, and central serotonergic systems. Exerc. Sport Sci. Rev. 39, 140-149.
25. Haider, S., Khaliq, S., Ahmed, S.P., and Haleem, D.J. (2006). Long-term tryptophan administration enhances cognitive performance and increases 5HT metabolism in the hippocampus of female rats. Amino Acids 31, 421-425.
26. Haider, S., Khaliq, S., Tabassum, S., and Haleem, D.J. (2012). Role of somatodendritic and postsynaptic 5-HT 1A receptors on learning and memory functions in rats. Neurochem. Res. 37, 2161-2166.
27. Hannon, J. and Hoyer, D. (2008). Molecular biology of 5-HT receptors. Behav. Brain Res. 195, 198-213.
28. Hodges, H., Sowinski, P., Turner, J.J., and Fletcher, A. (1996). Comparison of the effects of the 5-HT 3 receptor antagonists WAY-100579 and ondansetron on spatial learning in the water maze in rats with excitotoxic lesions of the forebrain cholinergic projection system. Psychopharmacology (Berl) 125, 146-161.
29. Homberg, J.R. (2012). Serotonin and decision making processes. Neurosci. Biobehav. Rev. 36, 218-236.
30. Hoyer, D., Clarke, D.E., Fozard, J.R., Hartig, P.R., Martin, G.R., Mylecharane, E.J., Saxena, P.R., and Humphrey, P.P. (1994). International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol. Rev. 46, 157-203.
31. Hoyer, D., Hannon, J.P., and Martin, G.R. (2002). Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol. Biochem. Behav. 71, 533-554.
32. Kandel, E.R. (2001). The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038.
33. Jacobs, B.L. and Azmitia, E.C. (1992). Structure and function of the brain serotonin system. Physiol. Rev. 72, 165-229.
34. Jans, L.A., Korte-Bouws, G.A., Korte, S.M., and Blokland, A. (2010). The effects of acute tryptophan depletion on affective behaviour and cognition in Brown Norway and Sprague Dawley rats. J. Psychopharmacol. 24, 605-614.
35. Konopka, W., Sch u tz, G., and Kaczmarek, L. (2011). The microRNA contribution to learning and memory. Neuroscientist 17, 468-474.
36. King, M.V., Marsden, C.A., and Fone, K.C. (2008). A role for the 5-HT 1A, 5-HT 4 and 5-HT 6 receptors in learning and memory. Trends Pharmacol. Sci. 29, 482-492.
37. Kristensen, M.O. (1990). Neurotransmitters in Alzheimer's disease. Ugeskr Laeger 152, 2165-2168.
38. Lacivita, E., Di Pilato, P., De Giorgio, P., Colabufo, N.A., Berardi, F., Perrone, R., and Leopoldo, M. (2012). The therapeutic potential of 5-HT 1A receptors: a patent review. Expert Opin. Ther. Pat. 22, 887-902.
39. Lancelot, S. and Zimmer, L. (2010). Small-animal positron emission tomography as a tool for neuropharmacology. Trends Pharmacol. Sci. 31, 411-417.
40. Lee, Y.A. and Goto, Y. (2011). Neurodevelopmental disruption of cortico-striatal function caused by degeneration of habenula neurons. PLoS One 6, e19450.
41. Leopoldo, M., Lacivita, E., Berardi, F., Perrone, R., and Hedlund, P.B. (2011). Serotonin 5-HT 7 receptor agents: structure-activity relationships and potential therapeutic applications in central nervous system disorders. Pharmacol. Ther. 129, 120-148.
42. Levkovitz, Y., Ophir-Shaham, O., Bloch, Y., Treves, I., Fennig, S., and Grauer, E. (2003). Effect of l-tryptophan on memory in patients with schizophrenia. J. Nerv. Ment. Dis. 191, 568-573.
43. Liu, X., Ramirez, S., Pang, P.T., Puryear, C.B., Govindarajan, A., Deisseroth, K., and Tonegawa, S. (2012). Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484, 381-385.
44. Mace, J.L., Porter, R.J., Dalrymple-Alford, J.C., Wesnes, K.A., and Anderson, T.J. (2010). Effects of acute tryptophan depletion on neuropsychological and motor function in Parkinson's disease. J. Psychopharmacol. 24, 1465-1472.
45. Maeda, J., Higuchi, M., and Suhara, T. (2009). Evaluation of imaging biomarker by transgenic mouse models. Nihon Shinkei Seishin Yakurigaku Zasshi 29, 73-78.
46. Mahgoub, M.A., Sara, Y., Kavalali, E.T., and Monteggia, L.M. (2006). Reciprocal interaction of serotonin and neuronal activity in regulation of cAMP-responsive element-dependent gene expression. J. Pharmacol. Exp. Ther. 317, 88-96.
47. Mancuso, C., Siciliano, R., Barone, E., Butterfield, D.A., and Preziosi, P. (2011). Pharmacologists and Alzheimer disease therapy: to boldly go where no scientist has gone before. Expert Opin. Investig. Drugs 20, 1243-1261.
48. Manuel-Apolinar, L., Rocha, L., Pascoe, D., Castillo, E., Castillo, C., and Meneses, A. (2005). Modifications of 5-HT 4 receptor expression in rat brain during memory consolidation. Brain Res. 1042, 73-81.
49. Marcos, B., Cabero, M., Solas, M., Aisa, B., and Ramirez, M.J. (2010). Signalling pathways associated with 5-HT 6 receptors: relevance for cognitive effects. Int. J. Neuropsychopharmacol. 13, 775-784.
50. Markowska, A.L., Stone, W.S., Ingram, D.K., Reynolds, J., Gold, P.E., Conti, L.H., Pontecorvo, M.J., Wenk, G.L., and Olton, D.S. (1989). Individual differences in aging: behavioral and neurobiological correlates. Neurobiol. Aging 10, 31-43.
51. Markstein, R., Matsumoto, M., Kohler, C., Togashi, H., Yoshioka, M., and Hoyer, D. (1999). Pharmacological characterization of 5-HT receptors positively coupled to adenylyl cyclase in the rat hippocampus. Naunyn Schmiedebergs Arch. Pharmacol. 359, 454-459.
52. Martel, J.C., Ormiere, A.M., Leduc, N., Assie, M.B., Cussac, D., and Newman-Tancredi, A. (2007). Native rat hippocampal 5-HT 1A receptors show constitutive activity. Mol Pharmacol. 71, 638-643.
53. Martorana, A., Esposito, Z., and Koch, G. (2010). Beyond the cholinergic hypothesis: do current drugs work in Alzheimer's disease? CNS Neurosci. Ther. 16, 235-245.
54. Meffre, J., Chaumont-Dubel, S., Mannoury la Cour, C., Loiseau, F., Watson, D.J., Dekeyne, A., Seveno, M., Rivet, J.M., Gaven, F., Deleris, P., et al. (2012). 5-HT6 receptor recruitment of mTOR as a mechanism for perturbed cognition in schizophrenia. EMBO Mol. Med. 4, 1043-1056.
55. Meltzer, C.C., Smith, G., Dekosky, S.T., Pollock, B.G., Mathis, C.A., Moore, R.Y., Kupfer, D.J., and Reynolds, C.F. (1998). Serotonin in aging, late-life depression and Alzheimer's disease: the emerging role of functional imaging. Neuropsychopharmacoloy 18, 407-430.
56. Meneses, A. (1999). 5-HT system and cognition. Neurosci. Biobehav. Rev. 23, 1111-1125.
57. Meneses, A. (2003). A pharmacological analysis of an associative learning task: 5-HT 1 to 5-HT 7 receptor subtypes function on a Pavlovian/instrumental autoshaped memory. Learn. Mem. 10, 363-372.
58. Meneses, A. (2007). Do serotonin 1-7 receptors modulate short and long-term memory? Neurobiol. Learn. Mem. 87, 561-72.
59. Meneses, A. and Perez-Garcia, G. (2007). 5-HT 1A receptors and memory. Neurosci. Biobehav. Rev. 31, 705-727.
60. Meneses, A., Manuel-Apolinar, L., Rocha, L., Castillo, E., and Castillo, C. (2004). Expression of the 5-HT receptors in rat brain during memory consolidation. Behav. Brain Res. 52, 425-436.
61. Meneses, A., P e rez-Garc i a, G., Ponce-Lopez, T., and Castillo, C. (2011a). 5-HT 6 receptor memory and amnesia: behavioral pharmacology - learning and memory processes. Int. Rev. Neurobiol. 96, 27-47.
62. Meneses, A., Perez-Garcia, G., Ponce-Lopez, T., Tellez, R., and Castillo, C. (2011b). Serotonin transporter and memory. Neuropharmacology 61, 355-363.
63. Meyer, J.H. (2012). Neuroimaging markers of cellular function in major depressive disorder: implications for therapeutics, personalized medicine, and prevention. Clin. Pharmacol. Ther. 91, 201-214.
64. Millan, M.J., Marin, P., Bockaert, J., and Mannoury la Cour, C. (2008). Signaling at G-protein-coupled serotonin receptors: recent advances and future research directions. Trends Pharmacol. Sci. 29, 454-464.
65. Millan, M.J., Agid, Y., Br u ne. M., Bullmore, E.T., Carter, C.S., Clayton, N.S., Connor, R., Davis, S., Deakin, B., DeRubeis, R.J., et al. (2012). Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy. Nat. Rev. Drug Discov. 11, 141-168.
66. Milner, T.A. and Veznedaroglu, E. (1993). Serotonin-containing terminals synapse on septohippocampal neurons in the rat. J. Neurosci. Res. 36, 260-271.
67. Mitchell, R.L. and Phillips, L.H. (2007). The psychological, neurochemical and functional neuroanatomical mediators of the effects of positive and negative mood on executive functions. Neuropsychologia 45, 617-29.
68. Morey, R.A., Hariri, A.R., Gold, A.L., Hauser, M.A., Munger, H.J., Dolcos, F., and McCarthy, G. (2011). Serotonin transporter gene polymorphisms and brain function during emotional distraction from cognitive processing in posttraumatic stress disorder. BMC Psychiatry 11, 76.
69. Murrough, J.W., Huang, Y., Hu, J., Henry, S., Williams, W., Gallezot, J.D., Bailey, C.R., Krystal, J.H., Carson, R.E., and Neumeister, A. (2011). Reduced amygdala serotonin transporter binding in posttraumatic stress disorder. Biol. Psychiatry 70, 1033-1038.
70. Ogren, S.O., Eriksson, T.M., Elvander-Tottie, E., D' Addario, C., Ekstr o m, J.C., Svenningsson, P., Meister, B., Kehr, J., and Stiedl, O. (2008). The role of 5-HT 1A receptors in learning and memory. Behav. Brain Res. 195, 54-77.
71. Ohno, Y. (2011). Therapeutic role of 5-HT 1A receptors in the treatment of schizophrenia and Parkinson's disease. CNS Neurosci. Ther. 17, 58-65.
72. Pacheco, J., Beevers, C.G., McGeary, J.E., and Schnyer, D.M. (2012). Memory monitoring performance and PFC activity are associated with 5-HTTLPR genotype in older adults. Neuropsychologia 50, 2257-2270.
73. Parrott, A.C. (2012). MDMA and 5-HT neurotoxicity: the empirical evidence for its adverse effects in humans - no need for translation. Br. J. Pharmacol. 166, 1518-1520.
74. Perez-Garcia, G. and Meneses, A. (2008). Memory formation, amnesia, improved memory and reversed amnesia: 5-HT role. Behav. Brain Res. 195, 17-29.
75. Perez-Garcia, G. and Meneses, A. (2009). Memory time-course: mRNA 5-HT 1A and 5-HT 7 receptors. Behav. Brain Res. 202, 102-113.
76. Porter, R.J., Lunn, R.S., and O'Brien, J.T. (2003). Effects of acute tryptophan depletion on cognitive function in Alzheimer's disease and in the healthy elderly. Psychol. Med. 33, 41-49.
77. Preskorn, S.H. (2012). The use of biomarkers in psychiatric research: how serotonin transporter occupancy explains the dose-response curves of SSRIs. J. Psychiatr. Pract. 18, 38-45.
78. Riedel, W.J., Klaassen, T., and Schmitt, J.A. (2002). Tryptophan, mood, and cognitive function. Brain Behav. Immun. 16, 581-589.
79. Roberts, A.J. and Hedlund, P.B. (2012). The 5-HT 7 receptor in learning and memory. Hippocampus 22, 762-771.
80. Rodr i guez, J.J., Noristani, H.N., and Verkhratsky, A. (2012). The serotonergic system in ageing and Alzheimer's disease. Prog. Neurobiol. 99, 15-41.
81. Romano, A.G., Quinn, J.L., Liu, R., Dave, K.D., Schwab, D., Alexander, G., Aloyo, V.J., and Harvey, J.A. (2006). Effect of serotonin depletion on 5-HT 2A -mediated learning in the rabbit: evidence for constitutive activity of the 5-HT 2A receptor in vivo. Psychopharmacology (Berl) 184, 173-181.
82. Roth, B.L., Hanizavareh, S.M., and Blum, A.E. (2004). Serotonin receptors represent highly favorable molecular targets for cognitive enhancement in schizophrenia and other disorders. Psychopharmacol. (Berl) 174, 17-24.
83. Ruiz, N.V. and Oranias, G.O. (2010). Patents. Int. Rev. Neurobiol. 94, 35-66.
84. Salmon, E. (2007). A review of the literature on neuroimaging of serotoninergic function in Alzheimer's disease and related disorders. J. Neural Transm. 114, 1179-1185.
85. Schmitt, J.A.J., Winger, M., Ramaekers, J.G., Evers, E.A.T., and Riedel, W.J. (2006). Serotonin and human cognitive performance. Curr. Pharm. Des. 12, 2473-2486.
86. Sghendo, L. and Mifsud, J. (2012). Understanding the molecular pharmacology of the serotonergic system: using fluoxetine as a model. J. Pharm. Pharmacol. 64, 317-325.
87. Sierksma, A.S., van den Hove, D.L., Steinbusch, H.W., and Prickaerts, J. (2010). Major depression, cognitive dysfunction and Alzheimer's disease: is there a link? Eur. J. Pharmacol. 626, 72-82.
88. Silber, B.Y. and Schmitt, J.A. (2010). Effects of tryptophan loading on human cognition, mood, and sleep. Neurosci. Biobehav. Rev. 34, 387-407.
89. Slotkin, T.A., MacKillop, E.A., Rudder, C.L., Ryde, I.T., Tate, C.A., and Seidler, F.J. (2007). Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions: indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age. Neuropsychopharmacology 32, 1082-1097.
90. Steckler, T. and Sahgal, A. (1995). The role of serotonergiccholinergic interactions in the mediation of cognitive behavior. Behav. Brain Res. 67, 165-199.
91. Steiner, B., Witte, V., and Fl o el, A. (2011). Lifestyle and cognition: what do we know from the aging and neurodegenerative brain? Nervenarzt 82, 1566-1577.
92. Str u der, H.K. and Weicker, H. (2001). Physiology and pathophysiology of the serotonergic system and its implications on mental and physical performance. Part I. Int. J. Sports Med. 22, 467-481.
93. Tassone, A., Madeo, G., Sciamanna, G., Pisani, A., and Bonsi, P. (2010). Electrophysiology of 5-HT 6 receptors. Int. Rev. Neurobiol. 94, 111-128.
94. Tellez, R., G o mez-V i quez, L., and Meneses, A. (2012a). GABA, glutamate, dopamine and serotonin transporters expression on memory formation and amnesia. Neurobiol. Learn. Mem. 97, 189-201.
95. Tellez, R., G o mez-Viquez, L., Liy-Salmeron, G., and Meneses, A. (2012b). GABA, glutamate, dopamine and serotonin transporters expression on forgetting. Neurobiol. Learn. Mem. 98, 66-77.
96. Terry, A.V. Jr, Buccafusco, J.J., and Wilson, C. (2008). Cognitive dysfunction in neuropsychiatric disorders: selected serotonin receptor subtypes as therapeutic targets. Behav Brain Res. 195, 30-38.
97. Thomasius, R., Zapletalova, P., Petersen, K., Buchert, R., Andresen, B., Wartberg, L., Nebeling, B., and Schmoldt, A. (2006). Mood, cognition and serotonin transporter availability in current and former ecstasy (MDMA) users: the longitudinal perspective. J. Psychopharmacol. 20, 211-225.
98. Toda, N., Kaneko, T., and Kogen, H. (2010). Development of an efficient therapeutic agent for Alzheimer's disease: design and synthesis of dual inhibitors of acetylcholinesterase and serotonin transporter. Chem. Pharm. Bull. (Tokyo) 58, 273-287.
99. Touma, C. (2011). Stress and affective disorders: animal models elucidating the molecular basis of neuroendocrine-behavior interactions. Pharmacopsychiatry 44 (Suppl 1), S15-26.
100. Vermetten, E. and Lanius, R.A. (2012). Biological and clinical framework for posttraumatic stress disorder. Handb. Clin. Neurol. 106, 291-342.
101. Woods, S., Clarke, N.N., Layfield, R., and Fone, K.C. (2012). 5-HT 6 receptor agonists and antagonists enhance learning and memory in a conditioned emotion response paradigm by modulation of cholinergic and glutamatergic mechanisms. Br. J. Pharmacol. 167, 436-449.
102. Youn, J., Misane, I., Eriksson, T.M., Millan, M.J., Ogren, S.O., Verhage, M., and Stiedl, O. (2009). Bidirectional modulation of classical fear conditioning in mice by 5-HT 1A receptor ligands with contrasting intrinsic activities. Neuropharmacology 57, 567-576.
103. Zangrossi, H. Jr., Viana, M.B., Zanoveli, J., Bueno, C., Nogueira, R.L., and Graeff, F.G. (2001). Serotonergic regulation of inhibitory avoidance and one-way escape in the rat elevated T-maze. Neurosci. Biobehav. Rev. 25, 637-645.