Social defeat: Impact on fear extinction and Amygdala-prefrontal cortical theta synchrony in 5-HTT deficient mice

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Narayanan, Venu ^a   Heiming, Rebecca S ^a   Jansen, Friederike ^a   Lesting, Jörg ^a   Sachser, Norbert ^a   Pape, Hans Christian ^a   Seidenbecher, Thomas ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONED REFLEX; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; EMOTION; FEAR; GENOTYPE; LATERAL AMYGDALA; LEARNING; MALE; MEDIAL PREFRONTAL CORTEX; MOUSE; NERVE CELL NETWORK; NONHUMAN; PREFRONTAL CORTEX; RECALL; REINFORCEMENT; SOCIAL BEHAVIOR; SOCIAL DEFEAT; THETA RHYTHM; ACTION POTENTIAL; AMYGDALOID NUCLEUS; ANIMAL; CATALEPSY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MUS;

ACTION POTENTIALS; AMYGDALA; ANIMALS; CORTICAL SYNCHRONIZATION; EXTINCTION, PSYCHOLOGICAL; FEAR; FREEZING REACTION, CATALEPTIC; GENOTYPE; MALE; MENTAL RECALL; MICE; MICE, KNOCKOUT; NERVE NET; PREFRONTAL CORTEX; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SOCIAL BEHAVIOR;

EID: 79960782040     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022600     Document Type: Article

References (99)

1. Holmes A, Murphy DL, Crawley JN, (2003) Abnormal behavioral phenotypes of serotonin transporter knockout mice: parallels with human anxiety and depression. Biol Psychiatry 54: 953-959.
2. Lucki I, O'Leary OF, (2004) Distinguishing roles for norepinephrine and serotonin in the behavioral effects of antidepressant drugs. J Clin Psychiatry 65 (Suppl 4): 11-24.
3. Lesch KP, Mossner R, (1998) Genetically driven variation in serotonin uptake: is there a link to affective spectrum, neurodevelopmental, and neurodegenerative disorders? Biol Psychiatry 44: 179-192.
4. Lesch KP, Mossner R, (1998) Knockout mice in neuropsychopharmacology: present and future. Int J Neuropsychopharmacol 1: 87-92.
5. Gross C, Hen R, (2004) Genetic and environmental factors interact to influence anxiety. Neurotox Res 6: 493-501.
6. Blakely RD, Berson HE, Fremeau RT Jr, Caron MG, Peek MM, et al. (1991) Cloning and expression of a functional serotonin transporter from rat brain. Nature 354: 66-70.
7. Murphy DL, Lerner A, Rudnick G, Lesch KP, (2004) Serotonin transporter: gene, genetic disorders, and pharmacogenetics. Mol Interv 4: 109-123.
8. Torres GE, Gainetdinov RR, Caron MG, (2003) Plasma membrane monoamine transporters: structure, regulation and function. Nat Rev Neurosci 4: 13-25.
9. Zahniser NR, Doolen S, (2001) Chronic and acute regulation of Na+/Cl--dependent neurotransmitter transporters: drugs, substrates, presynaptic receptors, and signaling systems. Pharmacol Ther 92: 21-55.
10. Torres GE, Amara SG, (2007) Glutamate and monoamine transporters: new visions of form and function. Curr Opin Neurobiol 17: 304-312.
11. Clement Y, Calatayud F, Belzung C, (2002) Genetic basis of anxiety-like behaviour: a critical review. Brain Res Bull 57: 57-71.
12. Lesch KP, (2004) Gene-environment interaction and the genetics of depression. J Psychiatry Neurosci 29: 174-184.
13. Arango V, Underwood MD, Boldrini M, Tamir H, Kassir SA, et al. (2001) Serotonin 1A receptors, serotonin transporter binding and serotonin transporter mRNA expression in the brainstem of depressed suicide victims. Neuropsychopharmacology 25: 892-903.
14. Ballenger JC, (1999) Current treatments of the anxiety disorders in adults. Biol Psychiatry 46: 1579-1594.
15. Briley MS, Raisman R, Sechter D, Zarifian E, Langer SZ, (1980) [3H]-Imipramine binding in human platelets: a new biochemical parameter in depression. Neuropharmacology 19: 1209-1210.
16. Gingrich JA, Hen R, (2001) Dissecting the role of the serotonin system in neuropsychiatric disorders using knockout mice. Psychopharmacology (Berl) 155: 1-10.
17. Malison RT, Price LH, Berman R, van Dyck CH, Pelton GH, et al. (1998) Reduced brain serotonin transporter availability in major depression as measured by [123I]-2 beta-carbomethoxy-3 beta-(4-iodophenyl)tropane and single photon emission computed tomography. Biol Psychiatry 44: 1090-1098.
18. Murphy DL, Wichems C, Li Q, Heils A, (1999) Molecular manipulations as tools for enhancing our understanding of 5-HT neurotransmission. Trends Pharmacol Sci 20: 246-252.
19. Nemeroff CB, Knight DL, Franks J, Craighead WE, Krishnan KR, (1994) Further studies on platelet serotonin transporter binding in depression. Am J Psychiatry 151: 1623-1625.
20. Kugaya A, Seneca NM, Snyder PJ, Williams SA, Malison RT, et al. (2003) Changes in human in vivo serotonin and dopamine transporter availabilities during chronic antidepressant administration. Neuropsychopharmacology 28: 413-420.
21. Stein DJ, Zungu-Dirwayi N, van Der Linden GJ, Seedat S, (2000) Pharmacotherapy for posttraumatic stress disorder. Cochrane Database Syst Rev.
22. Willeit M, Praschak-Rieder N, Neumeister A, Pirker W, Asenbaum S, et al. (2000) [123I]-beta-CIT SPECT imaging shows reduced brain serotonin transporter availability in drug-free depressed patients with seasonal affective disorder. Biol Psychiatry 47: 482-489.
23. Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, et al. (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274: 1527-1531.
24. Barr CS, Newman TK, Schwandt M, Shannon C, Dvoskin RL, et al. (2004) Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proc Natl Acad Sci USA 101: 12358-12363.
25. Bengel D, Murphy DL, Andrews AM, Wichems CH, Feltner D, et al. (1998) Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine ("Ecstasy") in serotonin transporter-deficient mice. Mol Pharmacol 53: 649-655.
26. Munafo MR, Clark T, Flint J, (2005) Does measurement instrument moderate the association between the serotonin transporter gene and anxiety-related personality traits? A meta-analysis. Mol Psychiatry 10: 415-419.
27. Lee JL, Di CP, Thomas KL, Everitt BJ, (2005) Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47: 795-801.
28. Mathews TA, Fedele DE, Coppelli FM, Avila AM, Murphy DL, et al. (2004) Gene dose-dependent alterations in extraneuronal serotonin but not dopamine in mice with reduced serotonin transporter expression. J Neurosci Methods 140: 169-181.
29. Kim DK, Tolliver TJ, Huang SJ, Martin BJ, Andrews AM, et al. (2005) Altered serotonin synthesis, turnover and dynamic regulation in multiple brain regions of mice lacking the serotonin transporter. Neuropharmacology 49: 798-810.
30. Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, et al. (2007) Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci 27: 684-691.
31. Holmes A, Yang RJ, Murphy DL, Crawley JN, (2002) Evaluation of antidepressant-related behavioral responses in mice lacking the serotonin transporter. Neuropsychopharmacology 27: 914-923.
32. Jansen F, Heiming RS, Lewejohann L, Touma C, Palme R, et al. (2010) Modulation of behavioural profile and stress response by 5-HTT genotype and social experience in adulthood. Behav Brain Res 207: 21-29.
33. Line SJ, Barkus C, Coyle C, Jennings KA, Deacon RM, et al. (2011) Opposing alterations in anxiety and species-typical behaviours in serotonin transporter overexpressor and knockout mice. EurNeuropsychopharmacol 21: 108-116.
34. Ansorge MS, Zhou M, Lira A, Hen R, Gingrich JA, (2004) Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 306: 879-881.
35. Holmes PV, (2003) Rodent models of depression: reexamining validity without anthropomorphic inference. Crit Rev Neurobiol 15: 143-174.
36. Murphy DL, Li Q, Engel S, Wichems C, Andrews A, et al. (2001) Genetic perspectives on the serotonin transporter. Brain Res Bull 56: 487-494.
37. Champagne FA, Curley JP, (2005) How social experiences influence the brain. Curr Opin Neurobiol 15: 704-709.
38. Kaiser S, Sachser N, (2005) The effects of prenatal social stress on behaviour: mechanisms and function. Neurosci Biobehav Rev 29: 283-294.
39. Buwalda B, Kole MH, Veenema AH, Huininga M, De Boer SF, et al. (2005) Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 29: 83-97.
40. Maren S, Quirk GJ, (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5: 844-852.
41. Pape HC, Pare D, (2010) Plastic synaptic networks of the amygdala for the acquisition expression, and extinction of conditioned fear. Physiol Rev in press.
42. Klimesch W, (1996) Memory processes, brain oscillations and EEG synchronization. Int J Psychophysiol 24: 61-100.
43. Pape HC, (2005) GABAergic neurons: gate masters of the amygdala, mastered by dopamine. Neuron 48: 877-879.
44. Pape HC, Driesang RB, (1998) Ionic mechanisms of intrinsic oscillations in neurons of the basolateral amygdaloid complex. J Neurophysiol 79: 217-226.
45. Pare D, Pape HC, Dong J, (1995) Bursting and oscillating neurons of the cat basolateral amygdaloid complex in vivo: electrophysiological properties and morphological features. J Neurophysiol 74: 1179-1191.
46. Seidenbecher T, Laxmi TR, Stork O, Pape HC, (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301: 846-850.
47. Sangha S, Narayanan RT, Bergado-Acosta JR, Stork O, Seidenbecher T, et al. (2009) Deficiency of the 65 kDa isoform of glutamic acid decarboxylase impairs extinction of cued but not contextual fear memory. J Neurosci 29: 15713-15720.
48. Adhikari A, Topiwala MA, Gordon JA, (2010) Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65: 257-269.
49. Lesting J, Narayanan T, Kluge C, Sangha S, Seidenbecher T, et al. (2011) Patterns of Coupled Theta Activity in Amygdala-Hippocampal-Prefrontal Cortical Circuits during Fear Extinction. PLoS One 6 (6): e21714 doi:21710.21371/journal.pone.0021714.
50. Heinz A, Braus DF, Smolka MN, Wrase J, Puls I, et al. (2005) Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nat Neurosci 8: 20-21.
51. Carroll JC, Boyce-Rustay JM, Millstein R, Yang R, Wiedholz LM, et al. (2007) Effects of mild early life stress on abnormal emotion-related behaviors in 5-HTT knockout mice. Beha Genet 37: 214-222.
52. Holmes A, (2001) Targeted gene mutation approaches to the study of anxiety-like behavior in mice. Neurosci Biobehav Rev 25: 261-273.
53. Heiming RS, Jansen F, Lewejohann L, Kaiser S, Schmitt A, et al. (2009) Living in a dangerous world: the shaping of behavioral profile by early environment and 5-HTT genotype. Front Behav Neurosci 3: 26.
54. Jennings KA, Loder MK, Sheward WJ, Pei Q, Deacon RM, et al. (2006) Increased expression of the 5-HT transporter confers a low-anxiety phenotype linked to decreased 5-HT transmission. J Neurosci 26: 8955-8964.
55. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders. 4th ed. Washington DC Amerycan Psychiatric Association pp. 424-429.
56. Grace AA, Rosenkranz JA, (2002) Regulation of conditioned responses of basolateral amygdala neurons. Physiol Behav 77: 489-493.
57. Pinto A, Jankowski M, Sesack SR, (2003) Projections from the paraventricular nucleus of the thalamus to the rat prefrontal cortex and nucleus accumbens shell: ultrastructural characteristics and spatial relationships with dopamine afferents. J Comp Neurol 459: 142-155.
58. Holmes A, Wellman CL, (2009) Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 33: 773-783.
59. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, et al. (2005) 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 8: 828-834.
60. Hariri AR, Drabant EM, Munoz KE, Kolachana BS, Mattay VS, et al. (2005) A susceptibility gene for affective disorders and the response of the human amygdala. Arch Gen Psychiatry 62: 146-152.
61. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, et al. (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297: 400-403.
62. Buzsaki G, Leung LW, Vanderwolf CH, (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287: 139-171.
63. Pare D, Collins DR, Pelletier JG, (2002) Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci 6: 306-314.
64. Narayanan RT, Seidenbecher T, Kluge C, Bergado J, Stork O, et al. (2007) Dissociated theta phase synchronization in amygdalo- hippocampal circuits during various stages of fear memory. Eur J Neurosci 25: 1823-1831.
65. Narayanan RT, Seidenbecher T, Sangha S, Stork O, Pape HC, (2007) Theta resynchronization during reconsolidation of remote contextual fear memory. Neuroreport 18: 1107-1111.
66. Pelletier JG, Pare D, (2004) Role of amygdala oscillations in the consolidation of emotional memories. Biol Psychiatry 55: 559-562.
67. Lesting J, Geiger M, Narayanan RT, Pape HC, Seidenbecher T, (2011) Impaired extinction of fear and maintained amygdala-hippocampal theta synchrony in a mouse model of temporal lobe epilepsy. Epilepsia 52: 337-346.
68. Hammack SE, Guo JD, Hazra R, Dabrowska J, Myers KM, et al. (2009) The response of neurons in the bed nucleus of the stria terminalis to serotonin: implications for anxiety. Prog Neuropsychopharmacol Biol Psychiatry 33: 1309-1320.
69. Ma QP, Yin GF, Ai MK, Han JS, (1991) Serotonergic projections from the nucleus raphe dorsalis to the amygdala in the rat. Neurosci Lett 134: 21-24.
70. Steinbusch HW, Nieuwenhuys R, Verhofstad AA, van der KD, (1981) The nucleus raphe dorsalis of the rat and its projection upon the caudatoputamen. A combined cytoarchitectonic, immunohistochemical and retrograde transport study. J Physiol (Paris) 77: 157-174.
71. 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.
72. Savitz J, Lucki I, Drevets WC, (2009) 5-HT(1A) receptor function in major depressive disorder. Prog Neurobiol 88: 17-31.
73. Marrosu F, Fornal CA, Metzler CW, Jacobs BL, (1996) 5-HT1A agonists induce hippocampal theta activity in freely moving cats: role of presynaptic 5-HT1A receptors. Brain Res 739: 192-200.
74. Maru E, Takahashi LK, Iwahara S, (1979) Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving rat. Brain Res 163: 223-234.
75. Nitz DA, McNaughton BL, (1999) Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat. Learn Mem 6: 153-167.
76. Vertes RP, Kinney GG, Kocsis B, Fortin WJ, (1994) Pharmacological suppression of the median raphe nucleus with serotonin1A agonists, 8-OH-DPAT and buspirone, produces hippocampal theta rhythm in the rat. Neuroscience 60: 441-451.
77. Daws LC, Montanez S, Munn JL, Owens WA, Baganz NL, et al. (2006) Ethanol inhibits clearance of brain serotonin by a serotonin transporter-independent mechanism. J Neurosci 26: 6431-6438.
78. Hajos M, Gartside SE, Varga V, Sharp T, (2003) In vivo inhibition of neuronal activity in the rat ventromedial prefrontal cortex by midbrain-raphe nuclei: role of 5-HT1A receptors. Neuropharmacology 45: 72-81.
79. Puig MV, Artigas F, Celada P, (2005) Modulation of the activity of pyramidal neurons in rat prefrontal cortex by raphe stimulation in vivo: involvement of serotonin and GABA. Cereb Cortex 15: 1-14.
80. Fabre V, Beaufour C, Evrard A, Rioux A, Hanoun N, et al. (2000) Altered expression and functions of serotonin 5-HT1A and 5-HT1B receptors in knock-out mice lacking the 5-HT transporter. Eur J Neurosci 12: 2299-2310.
81. Gobbi G, Murphy DL, Lesch K, 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.
82. Li XB, Inoue T, Hashimoto S, Koyama T, (2001) Effect of chronic administration of flesinoxan and fluvoxamine on freezing behavior induced by conditioned fear. Eur J Pharmacol 425: 43-50.
83. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A, (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412: 150-157.
84. Julius D, (1998) Serotonin receptor knockouts: a moody subject. Proc Natl Acad Sci USA 95: 15153-15154.
85. Rainnie DG, (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82: 69-85.
86. Koyama S, Kubo C, Rhee JS, Akaike N, (1999) Presynaptic serotonergic inhibition of GABAergic synaptic transmission in mechanically dissociated rat basolateral amygdala neurons. J Physiol 518 (Pt 2): 525-538.
87. Koyama S, Matsumoto N, Murakami N, Kubo C, Nabekura J, et al. (2002) Role of presynaptic 5-HT1A and 5-HT3 receptors in modulation of synaptic GABA transmission in dissociated rat basolateral amygdala neurons. Life Sci 72: 375-387.
88. Marowsky A, Yanagawa Y, Obata K, Vogt KE, (2005) A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function. Neuron 48: 1025-1037.
89. Jungling K, Seidenbecher T, Sosulina L, Lesting J, Sangha S, et al. (2008) Neuropeptide S-mediated control of fear expression and extinction: role of intercalated GABAergic neurons in the amygdala. Neuron 59: 298-310.
90. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ, (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36: 529-538.
91. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, et al. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301: 386-389.
92. Flugge G, (1995) Dynamics of central nervous 5-HT1A-receptors under psychosocial stress. J Neurosci 15: 7132-7140.
93. Veenema AH, Bredewold R, Neumann ID, (2007) Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32: 437-450.
94. Caspi A, Moffitt TE, (2006) Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat Rev Neurosci 7: 583-590.
95. Neumeister A, Konstantinidis A, Stastny J, Schwarz MJ, Vitouch O, et al. (2002) Association between serotonin transporter gene promoter polymorphism (5HTTLPR) and behavioral responses to tryptophan depletion in healthy women with and without family history of depression. Arch Gen Psychiatry 59: 613-620.
96. Bartolomucci A, Carola V, Pascucci T, Puglisi-Allegra S, Cabib S, et al. (2010) Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice. Dis Model Mech 3: 459-470.
97. Nietzer SL, Bonn M, Jansen F, Heiming RS, Lewejohann L, et al. (2011) Serotonin transporter knockout and repeated social defeat stress: Impact on neuronal morphology and plasticity in limbic brain areas. Behav Brain Res 220: 42-54.
98. Franklin KBJ, Paxinos G, (1997) The mouse brain in stereotaxic coordinates. San Diego Academic Press.
99. Adhikari A, Sigurdsson T, Topiwala MA, Gordon JA, (2010) Cross-correlation of instantaneous amplitudes of field potential oscillations: a straightforward method to estimate the directionality and lag between brain areas. J Neurosci Methods 191: 191-200.