Serotonin in fear conditioning processes

Behavioural Brain Research

Volumn 277, Issue , 2015, Pages 68-77

  Bauer, Elizabeth P ^a  

^a Barnard College of Columbia University   (United States)

Author keywords

Amygdala; Fear conditioning; Serotonin

Indexed keywords

SEROTONIN; SEROTONIN AGONIST; SEROTONIN ANTAGONIST; SEROTONIN TRANSPORTER; SEROTONIN UPTAKE INHIBITOR;

ACUTE DRUG ADMINISTRATION; ANXIETY; ANXIETY DISORDER; ASSOCIATION; CONDITIONING; DEPRESSION; DISEASE ASSOCIATION; EMOTIONALITY; FEAR; GENETIC VARIABILITY; HETEROZYGOTE; HUMAN; MEMORY CONSOLIDATION; NEUROANATOMY; NEUROCHEMISTRY; NEUROMODULATION; NEUROPSYCHIATRY; NONHUMAN; REVIEW; SEROTONIN TRANSPORTER GENE; SEROTONINERGIC SYSTEM; TREATMENT RESPONSE; ANIMAL; LEARNING; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; REINFORCEMENT;

ANIMALS; ANXIETY; CONDITIONING (PSYCHOLOGY); EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; LEARNING; SEROTONIN;

EID: 84912071513     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.07.028     Document Type: Review

References (236)

1. Grillon C. Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology. Biol Psychiatry 2002, 52(10):958-975.
2. Milad M.R., et al. Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J Psychiatr Res 2008, 42(7):515-520.
3. Bezchlibnyk-Butler K., Aleksic I., Kennedy S.H. Citalopram-a review of pharmacological and clinical effects. J Psychiatry Neurosci 2000, 25(3):241-254.
4. Gorman J.M. Treating generalized anxiety disorder. J Clin Psychiatry 2003, 64(Suppl. 2):24-29.
5. Kent J.M., Coplan J.D., Gorman J.M. Clinical utility of the selective serotonin reuptake inhibitors in the spectrum of anxiety. Biol Psychiatry 1998, 44(9):812-824.
6. Sheehan D.V., et al. Serotonin in panic disorder and social phobia. Int Clin Psychopharmacol 1993, 8(Suppl. 2):63-77.
7. Stein D.J., Stahl S. Serotonin and anxiety: current models. Int Clin Psychopharmacol 2000, 15(Suppl. 2):S1-S6.
8. Cornea-Hebert V., et al. Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat. J Comp Neurol 1999, 409(2):187-209.
9. Mascagni F., McDonald A.J. A novel subpopulation of 5-HT type 3A receptor subunit immunoreactive interneurons in the rat basolateral amygdala. Neuroscience 2007, 144(3):1015-1024.
10. Rainnie D.G. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 1999, 82(1):69-85.
11. Hashimoto S., Inoue T., Koyama T. Effects of conditioned fear stress on serotonin neurotransmission and freezing behavior in rats. Eur J Pharmacol 1999, 378(1):23-30.
12. Kawahara H., et al. Psychological stress increases serotonin release in the rat amygdala and prefrontal cortex assessed by in vivo microdialysis. Neurosci Lett 1993, 162(1-2):81-84.
13. Yokoyama M., et al. Amygdalic levels of dopamine and serotonin rise upon exposure to conditioned fear stress without elevation of glutamate. Neurosci Lett 2005, 379(1):37-41.
14. Campeau S., Davis M. Involvement of subcortical and cortical afferents to the lateral nucleus of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 1995, 15(3 Pt 2):2312-2327.
15. LeDoux J.E., et al. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 1988, 8(7):2517-2529.
16. Kim J.J., Rison R.A., Fanselow M.S. Effects of amygdala: hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci 1993, 107(6):1093-1098.
17. Maren S., Fanselow M.S. Electrolytic lesions of the fimbria/fornix: dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiol Learn Mem 1997, 67(2):142-149.
18. Selden N.R., Everitt B.J., Robbins T.W. Telencephalic but not diencephalic noradrenaline depletion enhances behavioural but not endocrine measures of fear conditioning to contextual stimuli. Behav Brain Res 1991, 43(2):139-154.
19. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33(1):56-72.
20. Bouton M.E., et al. Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol Psychiatry 2006, 60(4):352-360.
21. Ji J., Maren S. Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 2007, 17(9):749-758.
22. Dudai Y. The neurobiology of consolidations, or, how stable is the engram?. Annu Rev Psychol 2004, 55:51-86.
23. McGaugh J.L. Memory-a century of consolidation. Science 2000, 287(5451):248-251.
24. LeDoux J.E. Evolution of human emotion: a view through fear. Prog Brain Res 2012, 195:431-442.
25. LeDoux J.E. The slippery slope of fear. Trends Cogn Sci 2013, 17(4):155-156.
26. LeDoux J.E. Coming to terms with fear. Proc Natl Acad Sci USA 2014, 111(8):2871-2878.
27. Damasio A., Damasio H., Tranel D. Persistence of feelings and sentience after bilateral damage of the insula. Cereb Cortex 2013, 23(4):833-846.
28. Feinstein J.S., et al. Fear and panic in humans with bilateral amygdala damage. Nat Neurosci 2013, 16(3):270-272.
29. Amorapanth P., LeDoux J.E., Nader K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci 2000, 3(1):74-79.
30. Bechara A., et al. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 1995, 269(5227):1115-1118.
31. Johansen J.P., et al. Molecular mechanisms of fear learning and memory. Cell 2011, 147(3):509-524.
32. Orsini C.A., Maren S. Neural and cellular mechanisms of fear and extinction memory formation. Neurosci Biobehav Rev 2012, 36(7):1773-1802.
33. Pape H.C., Pare D. Plastic synaptic networks of the amygdala for the acquisition: expression, and extinction of conditioned fear. Physiol Rev 2010, 90(2):419-463.
34. Pare D., Duvarci S. Amygdala microcircuits mediating fear expression and extinction. Curr Opin Neurobiol 2012, 22(4):717-723.
35. LeDoux J.E., et al. The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 1990, 10(4):1062-1069.
36. LeDoux J.E., Ruggiero D.A., Reis D.J. Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J Comp Neurol 1985, 242(2):182-213.
37. Quirk G.J., Repa C., LeDoux J.E. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron 1995, 15(5):1029-1039.
38. Repa J.C., et al. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 2001, 4(7):724-731.
39. Romanski L.M., et al. Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav Neurosci 1993, 107(3):444-450.
40. Blair H.T., et al. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 2001, 8(5):229-242.
41. Collins D.R., Pare D. Differential fear conditioning induces reciprocal changes in the sensory responses of lateral amygdala neurons to the CS(+) and CS(-). Learn Mem 2000, 7(2):97-103.
42. Hopkins D.A., Holstege G. Amygdaloid projections to the mesencephalon: pons and medulla oblongata in the cat. Exp Brain Res 1978, 32(4):529-547.
43. Veening J.G., Swanson L.W., Sawchenko P.E. The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain Res 1984, 303(2):337-357.
44. Ciocchi S., et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 2010, 468(7321):277-282.
45. Wilensky A.E., et al. Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 2006, 26(48):12387-12396.
46. Goosens K.A., Maren S. Pretraining NMDA receptor blockade in the basolateral complex: but not the central nucleus, of the amygdala prevents savings of conditional fear. Behav Neurosci 2003, 117(4):738-750.
47. Haubensak W., et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 2010, 468(7321):270-276.
48. Li H., et al. Experience-dependent modification of a central amygdala fear circuit. Nat Neurosci 2013, 16(3):332-339.
49. Dong H.W., Petrovich G.D., Swanson L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 2001, 38(1-2):192-246.
50. Pare D., Smith Y., Pare J.F. Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat: Phaseolus vulgaris-leucoagglutinin anterograde tracing at the light and electron microscopic level. Neuroscience 1995, 69(2):567-583.
51. Petrovich G.D., Swanson L.W. Projections from the lateral part of the central amygdalar nucleus to the postulated fear conditioning circuit. Brain Res 1997, 763(2):247-254.
52. Resstel L.B., et al. Anxiolytic-like effects induced by acute reversible inactivation of the bed nucleus of stria terminalis. Neuroscience 2008, 154(3):869-876.
53. Sullivan G.M., et al. Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 2004, 128(1):7-14.
54. Alheid G.F. Extended amygdala and basal forebrain. Ann N Y Acad Sci 2003, 985:185-205.
55. Dunn J.D., Williams T.J. Cardiovascular responses to electrical stimulation of the bed nucleus of the stria terminalis. J Comp Neurol 1995, 352(2):227-234.
56. Walker D.L., Davis M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 1997, 17(23):9375-9383.
57. Walker D.L., Toufexis D.J., Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 2003, 463(1-3):199-216.
58. Walker D.L., Davis M. Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr Lennart Heimer. Brain Struct Funct 2008, 213(1-2):29-42.
59. McNish K.A., Gewirtz J.C., Davis M. Evidence of contextual fear after lesions of the hippocampus: a disruption of freezing but not fear-potentiated startle. J Neurosci 1997, 17(23):9353-9360.
60. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992, 106(2):274-285.
61. Kheirbek M.A., et al. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 2013, 77(5):955-968.
62. Liu X., et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012, 484(7394):381-385.
63. Ramirez S., et al. Creating a false memory in the hippocampus. Science 2013, 341(6144):387-391.
64. Bannerman D.M., et al. Ventral hippocampal lesions affect anxiety but not spatial learning. Behav Brain Res 2003, 139(1-2):197-213.
65. Matus-Amat P., et al. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci 2004, 24(10):2431-2439.
66. Richmond M.A., et al. Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behav Neurosci 1999, 113(6):1189-1203.
67. Rudy J.W., Matus-Amat P. The ventral hippocampus supports a memory representation of context and contextual fear conditioning: implications for a unitary function of the hippocampus. Behav Neurosci 2005, 119(1):154-163.
68. Kjelstrup K.G., et al. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 2002, 99(16):10825-10830.
69. Fanselow M.S., Dong H.W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65(1):7-19.
70. Pitkanen A., et al. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 2000, 911:369-391.
71. Herry C., et al. Switching on and off fear by distinct neuronal circuits. Nature 2008, 454(7204):600-606.
72. McDonald A.J., Mascagni F., Guo L. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 1996, 71(1):55-75.
73. Vertes R.P. Interactions among the medial prefrontal cortex: hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 2006, 142(1):1-20.
74. Duvarci S., Bauer E.P., Pare D. The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J Neurosci 2009, 29(33):10357-10361.
75. Amano T., et al. The fear circuit revisited: contributions of the basal amygdala nuclei to conditioned fear. J Neurosci 2011, 31(43):15481-15489.
76. Duvarci S., Popa D., Pare D. Central amygdala activity during fear conditioning. J Neurosci 2011, 31(1):289-294.
77. Burgos-Robles A., Vidal-Gonzalez I., Quirk G.J. Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J Neurosci 2009, 29(26):8474-8482.
78. Sotres-Bayon F., et al. Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 2012, 76(4):804-812.
79. Falls W.A., Miserendino M.J., Davis M. Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J Neurosci 1992, 12(3):854-863.
80. Lee H., Kim J.J. Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J Neurosci 1998, 18(20):8444-8454.
81. Lin C.H., et al. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J Neurosci 2003, 23(23):8310-8317.
82. Parkes S.L., Westbrook R.F. The basolateral amygdala is critical for the acquisition and extinction of associations between a neutral stimulus and a learned danger signal but not between two neutral stimuli. J Neurosci 2010, 30(38):12608-12618.
83. Amano T., Unal C.T., Pare D. Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 2010, 13(4):489-494.
84. Milad M.R., Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002, 420(6911):70-74.
85. Senn V., et al. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 2014, 81(2):428-437.
86. Christianson J.P., et al. 5-hydroxytryptamine 2C receptors in the basolateral amygdala are involved in the expression of anxiety after uncontrollable traumatic stress. Biol Psychiatry 2010, 67(4):339-345.
87. Mo B., et al. Restraint stress increases serotonin release in the central nucleus of the amygdala via activation of corticotropin-releasing factor receptors. Brain Res Bull 2008, 76(5):493-498.
88. Rueter L.E., Jacobs B.L. A microdialysis examination of serotonin release in the rat forebrain induced by behavioral/environmental manipulations. Brain Res 1996, 739(1-2):57-69.
89. Yoshioka M., et al. Effects of conditioned fear stress on 5-HT release in the rat prefrontal cortex. Pharmacol Biochem Behav 1995, 51(2-3):515-519.
90. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38(8):1083-1152.
91. Gartside S.E., et al. Effects of (-)-tertatolol, (-)-penbutolol and (+/-)-pindolol in combination with paroxetine on presynaptic 5-HT function: an in vivo microdialysis and electrophysiological study. Br J Pharmacol 1999, 127(1):145-152.
92. McDonald A.J., Mascagni F. Neuronal localization of 5-HT type 2A receptor immunoreactivity in the rat basolateral amygdala. Neuroscience 2007, 146(1):306-320.
93. Araneda R., Andrade R. 5-Hydroxytryptamine2 and 5-hydroxytryptamine 1A receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience 1991, 40(2):399-412.
94. Davies M.F., et al. Two distinct effects of 5-hydroxytryptamine on single cortical neurons. Brain Res 1987, 423(1-2):347-352.
95. Guo J.D., et al. Bi-directional modulation of bed nucleus of stria terminalis neurons by 5-HT: molecular expression and functional properties of excitatory 5-HT receptor subtypes. Neuroscience 2009, 164(4):1776-1793.
96. Richardson-Jones J.W., et al. Serotonin-1A autoreceptors are necessary and sufficient for the normal formation of circuits underlying innate anxiety. J Neurosci 2011, 31(16):6008-6018.
97. Griebel G. 5-Hydroxytryptamine-interacting drugs in animal models of anxiety disorders: more than 30 years of research. Pharmacol Ther 1995, 65(3):319-395.
98. Handley S.L., McBlane J.W. Serotonin mechanisms in animal models of anxiety. Braz J Med Biol Res 1993, 26(1):1-13.
99. Sanchez C., Meier E. Behavioral profiles of SSRIs in animal models of depression: anxiety and aggression. Are they all alike?. Psychopharmacology (Berl) 1997, 129(3):197-205.
100. Vertes R.P.A. PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 1991, 313(4):643-668.
101. Stutzmann G.E., LeDoux J.E. GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: a mechanism for modulation of sensory inputs related to fear conditioning. J Neurosci 1999, 19(11):RC8.
102. Li Q., et al. Brain region-specific alterations of 5-HT2A and 5-HT2C receptors in serotonin transporter knockout mice. J Neurochem 2003, 84(6):1256-1265.
103. Commons K.G., Connolley K.R., Valentino R.J. A neurochemically distinct dorsal raphe-limbic circuit with a potential role in affective disorders. Neuropsychopharmacology 2003, 28(2):206-215.
104. Azmitia E.C., Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 1978, 179(3):641-667.
105. Zhong P., Yan Z. Differential regulation of the excitability of prefrontal cortical fast-spiking interneurons and pyramidal neurons by serotonin and fluoxetine. PLoS One 2011, 6(2):e16970.
106. McQuade R., Sharp T. Functional mapping of dorsal and median raphe 5-hydroxytryptamine pathways in forebrain of the rat using microdialysis. J Neurochem 1997, 69(2):791-796.
107. Corradetti R., et al. Serotonin blocks the long-term potentiation induced by primed burst stimulation in the CA1 region of rat hippocampal slices. Neuroscience 1992, 46(3):511-518.
108. Passani M.B., et al. Effects of DAU 6215: a novel 5-hydroxytryptamine3 (5-HT3) antagonist on electrophysiological properties of the rat hippocampus. Br J Pharmacol 1994, 112(2):695-703.
109. Alhaider A.A., Ageel A.M., Ginawi O.T. The quipazine- and TFMPP-increased conditioned avoidance response in rats: role of 5HT1C/5-HT2 receptors. Neuropharmacology 1993, 32(12):1427-1432.
110. Harvey J.A. Role of the serotonin 5-HT(2A) receptor in learning. Learn Mem 2003, 10(5):355-362.
111. Zhang G., et al. Stimulation of serotonin 2A receptors facilitates consolidation and extinction of fear memory in C57BL/6J mice. Neuropharmacology 2013, 64:403-413.
112. Ma T.C., Yu Q.H. Effect of 20(S)-ginsenoside-Rg2 and cyproheptadine on two-way active avoidance learning and memory in rats. Arzneimittelforschung 1993, 43(10):1049-1052.
113. Marner L., et al. Loss of serotonin 2A receptors exceeds loss of serotonergic projections in early Alzheimer's disease: a combined [11C]DASB and [18F]altanserin-PET study. Neurobiol Aging 2012, 33(3):479-487.
114. Meltzer C.C., et al. Serotonin in aging, late-life depression, and Alzheimer's disease: the emerging role of functional imaging. Neuropsychopharmacology 1998, 18(6):407-430.
115. Wagner M., et al. The His452Tyr variant of the gene encoding the 5-HT2A receptor is specifically associated with consolidation of episodic memory in humans. Int J Neuropsychopharmacol 2008, 11(8):1163-1167.
116. Celada P., et al. The hallucinogen DOI reduces low-frequency oscillations in rat prefrontal cortex: reversal by antipsychotic drugs. Biol Psychiatry 2008, 64(5):392-400.
117. Yoshida H., et al. Subtype specific roles of serotonin receptors in the spine formation of cortical neurons in vitro. Neurosci Res 2011, 71(3):311-314.
118. Peddie C.J., et al. Colocalisation of serotonin2A receptors with the glutamate receptor subunits NR1 and GluR2 in the dentate gyrus: an ultrastructural study of a modulatory role. Exp Neurol 2008, 211(2):561-573.
119. Xia Z., et al. A direct interaction of PSD-95 with 5-HT2A serotonin receptors regulates receptor trafficking and signal transduction. J Biol Chem 2003, 278(24):21901-21908.
120. Ciranna L. Serotonin as a modulator of glutamate- and GABA-mediated neurotransmission: implications in physiological functions and in pathology. Curr Neuropharmacol 2006, 4(2):101-114.
121. Hasuo H., Matsuoka T., Akasu T. Activation of presynaptic 5-hydroxytryptamine 2A receptors facilitates excitatory synaptic transmission via protein kinase C in the dorsolateral septal nucleus. J Neurosci 2002, 22(17):7509-7517.
122. Arvanov V.L., et al. A pre- and postsynaptic modulatory action of 5-HT and the 5-HT2A: 2C receptor agonist DOB on NMDA-evoked responses in the rat medial prefrontal cortex. Eur J Neurosci 1999, 11(8):2917-2934.
123. Chen A., Hough C.J., Li H. Serotonin type II receptor activation facilitates synaptic plasticity via N-methyl-D-aspartate-mediated mechanism in the rat basolateral amygdala. Neuroscience 2003, 119(1):53-63.
124. Weisstaub N.V., et al. Cortical 5-HT2A receptor signaling modulates anxiety-like behaviors in mice. Science 2006, 313(5786):536-540.
125. Davis M., et al. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010, 35(1):105-135.
126. Campbell B.M., Merchant K.M. Serotonin 2C receptors within the basolateral amygdala induce acute fear-like responses in an open-field environment. Brain Res 2003, 993(1-2):1-9.
127. de Mello Cruz A.P., et al. Behavioral effects of systemically administered MK-212 are prevented by ritanserin microinfusion into the basolateral amygdala of rats exposed to the elevated plus-maze. Psychopharmacology (Berl) 2005, 182(3):345-354.
128. Gibson E.L., Barnfield A.M., Curzon G. Evidence that mCPP-induced anxiety in the plus-maze is mediated by postsynaptic 5-HT2C receptors but not by sympathomimetic effects. Neuropharmacology 1994, 33(3-4):457-465.
129. Heisler L.K., et al. Serotonin 5-HT(2C) receptors regulate anxiety-like behavior. Genes Brain Behav 2007, 6(5):491-496.
130. Hensman R., et al. Effects of ritanserin on aversive classical conditioning in humans. Psychopharmacology (Berl) 1991, 104(2):220-224.
131. Burghardt N.S., et al. Acute selective serotonin reuptake inhibitors increase conditioned fear expression: blockade with a 5-HT(2C) receptor antagonist. Biol Psychiatry 2007, 62(10):1111-1118.
132. De Vry J. 5-HT1A receptor agonists: recent developments and controversial issues. Psychopharmacology (Berl) 1995, 121(1):1-26.
133. Lacivita E., et al. 5-HT1A receptor: an old target for new therapeutic agents. Curr Top Med Chem 2008, 8(12):1024-1034.
134. Gross C., et al. Altered fear circuits in 5-HT(1A) receptor KO mice. Biol Psychiatry 2000, 48(12):1157-1163.
135. Olivier B., et al. The 5-HT(1A) receptor knockout mouse and anxiety. Behav Pharmacol 2001, 12(6-7):439-450.
136. Ramboz S., et al. Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc Natl Acad Sci USA 1998, 95(24):14476-14481.
137. Li X.B., et al. Effect of chronic administration of flesinoxan and fluvoxamine on freezing behavior induced by conditioned fear. Eur J Pharmacol 2001, 425(1):43-50.
138. Nakamura K., Kurasawa M. Anxiolytic effects of aniracetam in three different mouse models of anxiety and the underlying mechanism. Eur J Pharmacol 2001, 420(1):33-43.
139. Borelli K.G., et al. Effects of inactivation of serotonergic neurons of the median raphe nucleus on learning and performance of contextual fear conditioning. Neurosci Lett 2005, 387(2):105-110.
140. Stiedl O., et al. Involvement of the 5-HT1A receptors in classical fear conditioning in C57BL/6J mice. J Neurosci 2000, 20(22):8515-8527.
141. Almada R.C., et al. Serotonergic mechanisms of the median raphe nucleus-dorsal hippocampus in conditioned fear: Output circuit involves the prefrontal cortex and amygdala. Behav Brain Res 2009, 203(2):279-287.
142. Gomes F.V., et al. Cannabidiol injected into the bed nucleus of the stria terminalis reduces the expression of contextual fear conditioning via 5-HT1A receptors. J Psychopharmacol 2012, 26(1):104-113.
143. Li X., et al. 5-HT1A receptor agonist affects fear conditioning through stimulations of the postsynaptic 5-HT1A receptors in the hippocampus and amygdala. Eur J Pharmacol 2006, 532(1-2):74-80.
144. Morrison K.E., Cooper M.A. A role for 5-HT1A receptors in the basolateral amygdala in the development of conditioned defeat in Syrian hamsters. Pharmacol Biochem Behav 2012, 100(3):592-600.
145. Levita L., et al. 5-hydroxytryptamine1A-like receptor activation in the bed nucleus of the stria terminalis: electrophysiological and behavioral studies. Neuroscience 2004, 128(3):583-596.
146. Tada K., et al. Endogenous 5-HT inhibits firing activity of hippocampal CA1 pyramidal neurons during conditioned fear stress-induced freezing behavior through stimulating 5-HT1A receptors. Hippocampus 2004, 14(2):143-147.
147. Ferreira R., Nobre M.J. Conditioned fear in low- and high-anxious rats is differentially regulated by cortical subcortical and midbrain 5-HT receptors. Neuroscience 2014, 268C:159-168.
148. Bush D.E., Sotres-Bayon F., LeDoux J.E. Individual differences in fear: isolating fear reactivity and fear recovery phenotypes. J Trauma Stress 2007, 20(4):413-422.
149. Goswami S., et al. Impact of predatory threat on fear extinction in Lewis rats. Learn Mem 2010, 17(10):494-501.
150. Harrell A.V., Allan A.M. Improvements in hippocampal-dependent learning and decremental attention in 5-HT(3) receptor overexpressing mice. Learn Mem 2003, 10(5):410-419.
151. Nevins M.E., Anthony E.W. Antagonists at the serotonin-3 receptor can reduce the fear-potentiated startle response in the rat: evidence for different types of anxiolytic activity?. J Pharmacol Exp Ther 1994, 268(1):248-254.
152. Kondo M., et al. The 5-HT3A receptor is essential for fear extinction. Learn Mem 2014, 21(1):1-4.
153. Park S.M., Williams C.L. Contribution of serotonin type 3 receptors in the successful extinction of cued or contextual fear conditioned responses: interactions with GABAergic signaling. Rev Neurosci 2012, 23(5-6):555-569.
154. Blakely R.D., et al. Cloning and expression of a functional serotonin transporter from rat brain. Nature 1991, 354(6348):66-70.
155. Lesch K.P., et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274(5292):1527-1531.
156. Katsuragi S., et al. Association between serotonin transporter gene polymorphism and anxiety-related traits. Biol Psychiatry 1999, 45(3):368-370.
157. Hariri A.R., et al. Serotonin transporter genetic variation and the response of the human amygdala. Science 2002, 297(5580):400-403.
158. Eker M.C., et al. Smaller hippocampus volume is associated with short variant of 5-HTTLPR polymorphism in medication-free major depressive disorder patients. Neuropsychobiology 2011, 63(1):22-28.
159. Pezawas L., et al. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 2005, 8(6):828-834.
160. Brocke B., et al. Serotonin transporter gene variation impacts innate fear processing: Acoustic startle response and emotional startle. Mol Psychiatry 2006, 11(12):1106-1112.
161. Garpenstrand H., et al. Human fear conditioning is related to dopaminergic and serotonergic biological markers. Behav Neurosci 2001, 115(2):358-364.
162. Klumpers F., et al. Genetic variation in serotonin transporter function affects human fear expression indexed by fear-potentiated startle. Biol Psychol 2012, 89(2):277-282.
163. Crisan L.G., et al. Genetic contributions of the serotonin transporter to social learning of fear and economic decision making. Soc Cogn Affect Neurosci 2009, 4(4):399-408.
164. Barkus C., et al. Variation in serotonin transporter expression modulates fear-evoked hemodynamic responses and theta-frequency neuronal oscillations in the amygdala. Biol Psychiatry 2013.
165. Narayanan V., et al. Social defeat: impact on fear extinction and amygdala-prefrontal cortical theta synchrony in 5-HTT deficient mice. PLoS One 2011, 6(7):e22600.
166. Wellman C.L., et al. Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci 2007, 27(3):684-691.
167. Glotzbach-Schoon E., et al. Contextual fear conditioning in virtual reality is affected by 5HTTLPR and NPSR1 polymorphisms: effects on fear-potentiated startle. Front Behav Neurosci 2013, 7:31.
168. Heitland I., et al. Human fear acquisition deficits in relation to genetic variants of the corticotropin releasing hormone receptor 1 and the serotonin transporter. PLoS One 2013, 8(5):e63772.
169. Champagne F.A., Curley J.P. How social experiences influence the brain. Curr Opin Neurobiol 2005, 15(6):704-709.
170. Gross C., Hen R. Genetic and environmental factors interact to influence anxiety. Neurotox Res 2004, 6(6):493-501.
171. Lesch K.P. Gene-environment interaction and the genetics of depression. J Psychiatry Neurosci 2004, 29(3):174-184.
172. Caspi A., et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301(5631):386-389.
173. Jansen F., et al. Modulation of behavioural profile and stress response by 5-HTT genotype and social experience in adulthood. Behav Brain Res 2010, 207(1):21-29.
174. Gyawali S., et al. Association of a polyadenylation polymorphism in the serotonin transporter and panic disorder. Biol Psychiatry 2010, 67(4):331-338.
175. Hartley C.A., et al. Serotonin transporter polyadenylation polymorphism modulates the retention of fear extinction memory. Proc Natl Acad Sci USA 2012, 109(14):5493-5498.
176. Stokes P.E., Holtz A. Fluoxetine tenth anniversary update: the progress continues. Clin Ther 1997, 19(5):1135-1250.
177. van der Kolk B.A., et al. Fluoxetine in posttraumatic stress disorder. J Clin Psychiatry 1994, 55(12):517-522.
178. Griebel G., et al. Behavioral effects of acute and chronic fluoxetine in Wistar-Kyoto rats. Physiol Behav 1999, 67(3):315-320.
179. Kurt M., Arik A.C., Celik S. The effects of sertraline and fluoxetine on anxiety in the elevated plus-maze test in mice. J Basic Clin Physiol Pharmacol 2000, 11(2):173-180.
180. Ravinder S., Pillai A.G., Chattarji S. Cellular correlates of enhanced anxiety caused by acute treatment with the selective serotonin reuptake inhibitor fluoxetine in rats. Front Behav Neurosci 2011, 5:88.
181. Silva R.C., Brandao M.L. Acute and chronic effects of gepirone and fluoxetine in rats tested in the elevated plus-maze: an ethological analysis. Pharmacol Biochem Behav 2000, 65(2):209-216.
182. Bodnoff S.R., et al. A comparison of the effects of diazepam versus several typical and atypical anti-depressant drugs in an animal model of anxiety. Psychopharmacology (Berl) 1989, 97(2):277-279.
183. Bagdy G., et al. Anxiety-like effects induced by acute fluoxetine: sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635. Int J Neuropsychopharmacol 2001, 4(4):399-408.
184. Dekeyne A., et al. Citalopram reduces social interaction in rats by activation of serotonin (5-HT)(2C) receptors. Neuropharmacology 2000, 39(6):1114-1117.
185. Belzung C., et al. An investigation of the mechanisms responsible for acute fluoxetine-induced anxiogenic-like effects in mice. Behav Pharmacol 2001, 12(3):151-162.
186. Feighner J.P., et al. Double-blind comparison of bupropion and fluoxetine in depressed outpatients. J Clin Psychiatry 1991, 52(8):329-335.
187. Fergusson D., et al. Association between suicide attempts and selective serotonin reuptake inhibitors: systematic review of randomised controlled trials. BMJ 2005, 330(7488):396.
188. Goldstein B.J., Goodnick P.J. Selective serotonin reuptake inhibitors in the treatment of affective disorders-III. Tolerability, safety and pharmacoeconomics. J Psychopharmacol 1998, 12(3 Suppl B):S55-S87.
189. Gorman J.M., et al. An open trial of fluoxetine in the treatment of panic attacks. J Clin Psychopharmacol 1987, 7(5):329-332.
190. Masand P.S., Gupta S. Selective serotonin-reuptake inhibitors: an update. Harv Rev Psychiatry 1999, 7(2):69-84.
191. Spigset O. Adverse reactions of selective serotonin reuptake inhibitors: reports from a spontaneous reporting system. Drug Saf 1999, 20(3):277-287.
192. Teicher M.H., Glod C., Cole J.O. Emergence of intense suicidal preoccupation during fluoxetine treatment. Am J Psychiatry 1990, 147(2):207-210.
193. Blier P., Bergeron R. Effectiveness of pindolol with selected antidepressant drugs in the treatment of major depression. J Clin Psychopharmacol 1995, 15(3):217-222.
194. Gardier A.M., et al. Role of 5-HT1A autoreceptors in the mechanism of action of serotoninergic antidepressant drugs: recent findings from in vivo microdialysis studies. Fundam Clin Pharmacol 1996, 10(1):16-27.
195. Riaza Bermudo-Soriano C., et al. New perspectives in glutamate and anxiety. Pharmacol Biochem Behav 2012, 100(4):752-774.
196. Sanacora G., Treccani G., Popoli M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 2012, 62(1):63-77.
197. Skolnick P., et al. Adaptation of N-methyl-D-aspartate (NMDA) receptors following antidepressant treatment: implications for the pharmacotherapy of depression. Pharmacopsychiatry 1996, 29(1):23-26.
198. Bosker F.J., et al. Acute and chronic effects of citalopram on postsynaptic 5-hydroxytryptamine(1A) receptor-mediated feedback: a microdialysis study in the amygdala. J Neurochem 2001, 76(6):1645-1653.
199. Hervas I., et al. Role of uptake inhibition and autoreceptor activation in the control of 5-HT release in the frontal cortex and dorsal hippocampus of the rat. Br J Pharmacol 2000, 130(1):160-166.
200. Invernizzi R., et al. Effect of 5-HT1A receptor antagonists on citalopram-induced increase in extracellular serotonin in the frontal cortex, striatum and dorsal hippocampus. Neuropharmacology 1997, 36(4-5):467-473.
201. Burghardt N.S., et al. The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biol Psychiatry 2004, 55(12):1171-1178.
202. Gravius A., et al. The role of group I metabotropic glutamate receptors in acquisition and expression of contextual and auditory fear conditioning in rats-a comparison. Neuropharmacology 2006, 51(7-8):1146-1155.
203. Ravinder S., et al. A role for the extended amygdala in the fear-enhancing effects of acute selective serotonin reuptake inhibitor treatment. Transl Psychiatry 2013, 3:e209.
204. Grillon C., Levenson J., Pine D.S. A single dose of the selective serotonin reuptake inhibitor citalopram exacerbates anxiety in humans: a fear-potentiated startle study. Neuropsychopharmacology 2007, 32(1):225-231.
205. Lino-de-Oliveira C., et al. Effects of acute and chronic fluoxetine treatments on restraint stress-induced Fos expression. Brain Res Bull 2001, 55(6):747-754.
206. Morelli M., et al. Induction of Fos-like-immunoreactivity in the central extended amygdala by antidepressant drugs. Synapse 1999, 31(1):1-4.
207. Singewald N., Salchner P., Sharp T. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol Psychiatry 2003, 53(4):275-283.
208. Veening J.G., et al. Patterns of c-fos expression induced by fluvoxamine are different after acute vs chronic oral administration. Eur Neuropsychopharmacol 1998, 8(3):213-226.
209. Hashimoto S., et al. Effects of acute citalopram on the expression of conditioned freezing in naive versus chronic citalopram-treated rats. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33(1):113-117.
210. Inoue T., et al. Effect of citalopram: a selective serotonin reuptake inhibitor, on the acquisition of conditioned freezing. Eur J Pharmacol 1996, 311(1):1-6.
211. Montezinho L.P., et al. The effects of acute treatment with escitalopram on the different stages of contextual fear conditioning are reversed by atomoxetine. Psychopharmacology (Berl) 2010, 212(2):131-143.
212. Hashimoto S., Inoue T., Koyama T. Serotonin reuptake inhibitors reduce conditioned fear stress-induced freezing behavior in rats. Psychopharmacology (Berl) 1996, 123(2):182-186.
213. Muraki I., Inoue T., Koyama T. Effect of co-administration of the selective 5-HT1A receptor antagonist WAY 100,635 and selective 5-HT1B/1D receptor antagonist GR 127,935 on anxiolytic effect of citalopram in conditioned fear stress in the rat. Eur J Pharmacol 2008, 586(1-3):171-178.
214. Santos J.M., Martinez R.C., Brandao M.L. Effects of acute and subchronic treatments with fluoxetine and desipramine on the memory of fear in moderate and high-intensity contextual conditioning. Eur J Pharmacol 2006, 542(1-3):121-128.
215. Igelstrom K.M., Heyward P.M. Inhibition of hippocampal excitability by citalopram. Epilepsia 2012, 53(11):2034-2042.
216. Staubli U., Otaky N. Serotonin controls the magnitude of LTP induced by theta bursts via an action on NMDA-receptor-mediated responses. Brain Res 1994, 643(1-2):10-16.
217. Anagnostaras S.G., Gale G.D., Fanselow M.S. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 2001, 11(1):8-17.
218. Frankland P.W., et al. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 1998, 112(4):863-874.
219. Burghardt N.S., et al. Chronic antidepressant treatment impairs the acquisition of fear extinction. Biol Psychiatry 2012.
220. Lebron-Milad K., et al. Sex differences and estrous cycle in female rats interact with the effects of fluoxetine treatment on fear extinction. Behav Brain Res 2013, 253:217-222.
221. Young S.N., et al. Tryptophan depletion causes a rapid lowering of mood in normal males. Psychopharmacology (Berl) 1985, 87(2):173-177.
222. Fadda F., et al. A tryptophan-free diet markedly reduces frontocortical 5-HT release: but fails to modify ethanol preference in alcohol-preferring (sP) and non-preferring (sNP) rats. Behav Brain Res 2000, 108(2):127-132.
223. Stancampiano R., et al. Acute administration of a tryptophan-free amino acid mixture decreases 5-HT release in rat hippocampus in vivo. Am J Physiol 1997, 272(3 Pt 2):R991-R994.
224. Jequier E., Lovenberg W., Sjoerdsma A. Tryptophan hydroxylase inhibition: the mechanism by which p-chlorophenylalanine depletes rat brain serotonin. Mol Pharmacol 1967, 3(3):274-278.
225. Baumgarten H.G., Bjorklund A. Neurotoxic indoleamines and monoamine neurons. Annu Rev Pharmacol Toxicol 1976, 16:101-111.
226. Robinson O.J., et al. Acute tryptophan depletion increases translational indices of anxiety but not fear: serotonergic modulation of the bed nucleus of the stria terminalis?. Neuropsychopharmacology 2012, 37(8):1963-1971.
227. Uchida S., et al. Brain neurotransmitter receptor-binding characteristics in rats after oral administration of haloperidol: risperidone and olanzapine. Life Sci 2007, 80(17):1635-1640.
228. Hughes C.R., Keele N.B. Phenytoin normalizes exaggerated fear behavior in p-chlorophenylalanine (PCPA)-treated rats. Epilepsy Behav 2006, 9(4):557-563.
229. Inoue T. Effects of conditioned fear stress on monoaminergic systems in the rat brain. Hokkaido Igaku Zasshi 1993, 68(3):377-390.
230. Hindi Attar C., Finckh B., Buchel C. The influence of serotonin on fear learning. PLoS One 2012, 7(8):e42397.
231. Roiser J.P., et al. The effects of acute tryptophan depletion and serotonin transporter polymorphism on emotional processing in memory and attention. Int J Neuropsychopharmacol 2007, 10(4):449-461.
232. Lothe A., et al. Association between triallelic polymorphism of the serotonin transporter and [18F]MPPF binding potential at 5-HT1A receptors in healthy subjects. Neuroimage 2009, 47(2):482-492.
233. Jasnow A.M., et al. Thy1-expressing neurons in the basolateral amygdala may mediate fear inhibition. J Neurosci 2013, 33(25):10396-10404.
234. Benzekhroufa K., et al. Adenoviral vectors for highly selective gene expression in central serotonergic neurons reveal quantal characteristics of serotonin release in the rat brain. BMC Biotechnol 2009, 9:23.
235. Benzekhroufa K., et al. Targeting central serotonergic neurons with lentiviral vectors based on a transcriptional amplification strategy. Gene Ther 2009, 16(5):681-688.
236. Fenno L., Yizhar O., Deisseroth K. The development and application of optogenetics. Annu Rev Neurosci 2011, 34:389-412.