Pavlovian fear memory circuits and phenotype models of PTSD

Neuropharmacology

Volumn 62, Issue 2, 2012, Pages 638-646

  Johnson, Luke R ^a,b,c   McGuire, Jennifer ^a,c   Lazarus, Rachel ^a   Palmer, Abraham A ^d  

^a Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

^b Center for the Study of Traumatic Stress (CSTS)   (United States)

^c Center for Neuroscience and Regenerative Medicine (CNRM)   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

Amygdala; Classical conditioning; Hippocampus; Micro anatomy; Post traumatic stress disorder; QTL

Indexed keywords

CYCLIC AMP; MITOGEN ACTIVATED PROTEIN KINASE 1; SEROTONIN TRANSPORTER;

AUTONOMIC NERVOUS SYSTEM FUNCTION; BDNF GENE; BEHAVIOR THERAPY; DEFENSIVE BEHAVIOR; DISEASE ASSOCIATION; EPIGENETICS; FEAR; GENE; GENETIC PREDISPOSITION; GENETIC RISK; GENETIC VARIABILITY; HERITABILITY; HIGH RISK POPULATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MEMORY CONSOLIDATION; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NONHUMAN; PAIN THRESHOLD; PAVLOVIAN FEAR CONDITIONING; PHENOTYPE; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS MAPPING; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; ASSOCIATION LEARNING; BRAIN; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; FEAR; NERVE NET; PHENOTYPE; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84855968536     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.07.004     Document Type: Review

References (101)

1. S.G. Anagnostaras, G.D. Gale, and M.S. Fanselow Hippocampus and contextual fear conditioning: recent controversies and advances Hippocampus 11 2001 8 17
2. A.B. Amstadter, N.R. Nugent, and K.C. Koenen Genetics of PTSD: fear conditioning as a model for future research Psychiatr. Ann. 39 6 2009 358 367
3. J.L. Armony, G.J. Quirk, and J.E. LeDoux Differential effects of amygdala lesions on early and late plastic components of auditory cortex spike trains during fear conditioning J. Neurosci. 18 1998 2592 2601
4. J.L. Armony, D. Servan-Schreiber, J.D. Cohen, and J.E. LeDoux An anatomically constrained neural network model of fear conditioning Behav. Neurosci. 109 1995 246 257
5. J.N. Bailey, A.K. Goenjian, E.P. Noble, D.P. Walling, T. Ritchie, and H.A. Goenjian PTSD and dopaminergic genes DRD2 and DAT, in multigenerational families exposed to the Spitak earthquake Psychiatry Res. 178 2010 507 510
6. S.A. Balogh, and J.M. Wehner Inbred mouse strain differences in the establishment of long-term fear memory Behav. Brain Res. 140 1-2 2003 97 106
7. E.P. Bauer, J.E. LeDoux, and K. Nader Fear conditioning and LTP in the lateral amygdala are sensitive to the same stimulus contingencies Nat. Neurosci. 4 7 2001 687 688 Jul
8. H.C. Bergstrom, C.G. McDonald, and L.R. Johnson Pavlovian fear conditioning activates a common pattern of neurons in the lateral amygdala of individual brains PLoS One 6 Issue 1 2011 e15698 January
9. J.F. Bernard, and J.M. Besson The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes J. Neurophysiol. 63 1990 473 490
10. J.F. Bernard, G.F. Huang, and J.M. Besson Effect of noxious somesthetic stimulation on the activity of neurons of the nucleus centralis of the amygdala Brain Res. 523 1990 347 350
11. J. Blechert, T. Michael, N. Vriends, J. Margraf, and F.H. Wilhelm Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses Psychol. Med. 35 6 2005 791 806
12. J.D. Bremner, E. Vermetten, C. Schmahl, V. Vaccarino, M. Vythilingam, N. Afzal, C. Grillon, and D.S. Charney Positron emission tomographic imaging of neural correlates of a fear acquisition and extinction paradigm in women with childhood sexual-abuse-related post-traumatic stress disorder Psychol. Med. 35 6 2005 791 806 Jun
13. J.L. Brigman, P. Mathur, L. Lu, R.W. Williams, and A. Holmes Genetic relationship between anxiety-related and fear-related behaviors in BXD recombinant inbred mice Behav. Pharmacol. 20 2 2009 204 209
14. B. Caldarone, C. Saavedra, K. Tartaglia, J.M. Wehner, B.C. Dudek, and L. Flaherty Quantitative trait loci analysis affecting contextual conditioning in mice Nat. Genet. 17 3 1997 335 357
15. M. Camp, M. Norcross, N. Whittle, M. Feyder, W. D'Hanis, D. Yilmazer-Hanke, N. Singewald, and A. Holmes Impaired Pavlovian fear extinction is a common phenotype across genetic lineages of the 129 inbred mouse strain Genes Brain Behav. 8 8 2009 744 752
16. H. Cohen, A.B. Geva, M.A. Matar, J. Zohar, and Z. Kaplan Post-traumatic stress behavioural responses in inbred mouse strains: can genetic predisposition explain phenotypic vulnerability? Int. J. Neuropsychopharmacol. 3 2008 331 349
17. M.C. Cornelis, N.R. Nugent, A.B. Amstadter, and K.C. Koenen Genetics of post-traumatic stress disorder: review and recommendations for genome-wide association studies Curr. Psychiatry Rep. 12 2010 313 326
18. M. Davis The role of the amygdala in fear and anxiety Annu. Rev. Neurosci. 15 1992 353 375
19. J. Dbiec, D.E. Bush, and J.E. LeDoux Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats-a possible mechanism for the persistence of traumatic memories in PTSD Depress. Anxiety 28 3 2011 186 193 Mar
20. M.R. Delgado, A. Olsson, and E.A. Phelps Extending animal models of fear conditioning to humans Biol. Psychol. 73 1 2006 39 48 Jul
21. V. Doyere, J. Debiec, M.H. Monfils, G.E. Schafe, and J.E. LeDoux Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala Nat. Neurosci. 10 2007 414 416
22. D.W. DuBois, A. Perlegas, D.W. Floyd, J.L. Weiner, and B.A. McCool Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57/B6 and DBA/J2 mice J. Pharmacol. Exp. Ther. 318 23 2006 629 640
23. B.M. Elzinga, and J.D. Bremner Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? J. Affect.J. Consult. Clin. Psychol. Disord. 70 1 2002 1 17 Jun
24. N. Essar, Y. Palgi, R. Saar, and M. Ben-Ezra Pre-traumatic vaccination intervention: can dissociative symptoms be reduced? Prehosp. Disaster Med. 25 3 2010 278 284
25. M.S. Fanselow, and J.E. LeDoux Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala Neuron 23 1999 229 232
26. E.B. Foa, C. Molnar, and L. Cashman Change in rape narratives during exposure therapy for posttraumatic stress disorder J. Trauma Stress 8 4 1995 675 690
27. H. Frielingsdorf, K.G. Bath, F. Soliman, J. Difede, B.J. Casey, and F.S. Lee Variant brain-derived neurotrophic factor Val66Met endophenotypes: implications for posttraumatic stress disorder Ann. N. Y. Acad. Sci. 1208 2010 150 157
28. A.K. Goenjian, E.P. Noble, P.W. Walling, H.A. Goenjian, I.S. Karayan, T. Ritchie, and J.N. Bailey Heritabilities of symptoms of posttraumatic stress disorder, anxiety and depression in earthquake exposed Armenian families Psychiatr. Genet. 18 2008 261 266
29. S.L. Halligan, T. Michael, D.M. Clark, and A. Ehlers Posttraumatic stress disorder following assault: the role of cognitive processing, trauma memory, and appraisals J. Consult. Clin. Psychol. 71 3 2003 419 431
30. J.H. Han, S.A. Kushner, A.P. Yiu, C.J. Cole, A. Matynia, R.A. Brown, R.L. Neve, J.F. Guzowski, A.J. Silva, and S.A. Josselyn Neuronal competition and selection during memory formation Science 316 5823 2007 457 460
31. D. Hauer, F. Weis, A. Papassotiropoulos, M. Schmoeckel, A. Beiras-Fernandez, J. Lieke, I. Kaufmann, F. Kirchhoff, M. Vogeser, B. Roozendaal, J. Briegel, D. de Quervain, and G. Schelling Relationship of a common polymorphism of the glucocorticoid receptor gene to traumatic memories and posttraumatic stress disorder in patients after intensive care therapy Crit. Care Med. 39 4 2011 643 650 Apr
32. C. Herry, S. Ciocchi, V. Senn, L. Demmou, C. Muller, and A. Luthi Switching on and off fear by distinct neuronal circuits Nature 454 2008 600 606
33. J.M. Hettema, P. Annas, M.C. Neale, M. Fredrikson, and K.S. Kendler The genetic covariation between fear conditioning and self-report fears Biol. Psychiatry 63 6 2008 587 593
34. J.M. Hettema, P. Annas, M.C. Neale, K.S. Kendler, and M. Fredrikson A twin study of the genetics of fear conditioning Arch. Gen. Psychiatry 60 7 2003 702 708
35. A. Holmes, C.C. Wrenn, A.P. Harris, K.E. Thayer, and J.N. Crawley Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice Genes Brain Behav. 1 1 2002 55 69
36. Y. Humeau, C. Herry, N. Kemp, H. Shaban, E. Fourcaudot, S. Bissiere, and A. Luthi Dendritic spine heterogeneity determines afferent-specific Hebbian plasticity in the amygdala Neuron 45 2005 119 131
37. A. Izquierdo, C.L. Wellman, and A. Holmes Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice J. Neurosci. 26 21 2006 5733 5738 May 24
38. S.A. Josselyn, C. Shi, W.A. Carlezon Jr., R.L. Neve, E.J. Nestler, and M. Davis Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala J. Neurosci. 21 7 2001 2404 2412
39. T. Jovanovic, and K.J. Ressler How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD Am. J. Psychiatry 167 6 2010 648 662
40. L.R. Johnson, and J.E. LeDoux The anatomy of fear: microcircuits of the lateral amygdala J.M. Gorman, In Fear and Anxiety: The Benefits of Translational Research 2004 APPA Press Washington D.C 227 250
41. L.R. Johnson, M. Hou, A. Ponce-Alvarez, L.M. Gribelyuk, H.H. Alphs, L. Albert, B.L. Brown, J.E. Ledoux, and V. Doyere A recurrent network in the lateral amygdala: a mechanism for coincidence detection Front. Neural Circuits 2 2008 3
42. L.R. Johnson, J.E. LeDoux, and V. Doyere Hebbian reverberations in emotional memory micro circuits Front. Neurosci. 3 2 2009 198 205
43. L.R. Johnson, and J.E. LeDoux Amygdala microcircuitry G. Shepard, S. Griller, Brain Microcircuits 2010 Oxford University Press
44. A. Kelly, S. Laroche, and S. Davis Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory J. Neurosci. 23 12 2003 5354 5360
45. K.C. Koenen, A.B. Amstadter, and N.R. Nugent Gene-environment interaction in posttraumatic stress disorder: an update J. Trauma Stress 2009 Sep 9
46. E. Lanuza, J. Moncho-Bogani, and J.E. Ledoux Unconditioned stimulus pathways to the amygdala: effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala Neuroscience 155 2008 959 968
47. J. LeDoux The emotional brain, fear, and the amygdala Cell Mol. Neurobiol. 23 2003 727 738
48. J. LeDoux The amygdala Curr. Biol. 17 2007 R868 R874
49. J.E. LeDoux Emotion, memory and the brain Sci. Am. 270 1994 50 57
50. J.E. LeDoux Emotion circuits in the brain Annu. Rev. Neurosci. 23 2000 155 184
51. X.F. Li, G.E. Stutzmann, and J.E. LeDoux Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways Learn. Mem. 3 1996 229 242
52. S. Lissek, A.S. Powers, E.B. McClure, E.A. Phelps, G. Woldehawariat, C. Grillon, and D.S. Pine Classical fear conditioning in the anxiety disorders: a meta-analysis Behav. Res. Ther. 43 11 2005 1391 1424
53. R. Lopez-Aumatell, M. Guitart-Masip, E. Vicens-Costa, L. Gimenez-Llort, W. Valdar, M. Johannesson, J. Flint, A. Tobeña, and A. Fernandez-Teruel Fearfulness in a large N/Nih genetically heterogeneous rat stock: differential profiles of timidity and defensive flight in males and females Behav. Brain Res. 188 1 2008 41 55
54. R.E. Lubow, and A.U. Moore Latent inhibition: the effect of nonreinforced pre-exposure to the conditional stimulus J. Comp. Physiol. Psychol. 52 1959 415 419
55. S. Maren, and G.J. Quirk Neuronal signalling of fear memory Nat. Rev. Neurosci. 5 2004 844 852
56. J.A. McCaughran Jr., J. Bell 3rd, and R.J. Hitzemann Fear-potentiated startle response in mice: genetic analysis of the C57BL/6J and DBA/2J intercross Pharmacol. Biochem. Behav. 65 2 2000 301 312
57. M.G. McKernan, and P. Shinnick-Gallagher Fear conditioning induces a lasting potentiation of synaptic currents in vitro Nature 390 1997 607 611
58. M.R. Milad, and G.J. Quirk Neurons in medial prefrontal cortex signal memory for fear extinction Nature 420 2002 70 74
59. M.R. Milad, R.K. Pitman, C.B. Ellis, A.L. Gold, L.M. Shin, N.B. Lasko, M.A. Zeidan, K. Handwerger, S.P. Orr, and S.L. Rauch Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder Biol. Psychiatry 66 12 2009 1075 1082 Dec 15, Epub 2009 Sep 12
60. M.J. Miserendino, C.B. Sananes, K.R. Melia, and M. Davis Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala Nature 345 1990 716 718
61. M.H. Monfils, K.K. Cowansage, E. Klann, and J.E. LeDoux Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories Science 324 5929 2009 951 955
62. M.A. Morgan, and J.E. LeDoux Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats Neurobiol. Learn. Mem. 72 3 1999 244 251
63. M.A. Morgan, L.M. Romanski, and J.E. LeDoux Extinction of emotional learning: contribution of medial prefrontal cortex Neurosci. Lett. 163 1993 109 113
64. K.M. Myers, and M. Davis Mechanisms of fear extinction Mol. Psychiatry 12 2007 120 150
65. K. Nader, G.E. Schafe, and J.E. Le Doux Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval Nature 406 6797 2000 722 726
66. S.D. Norrholm, T. Jovanovic, I.W. Olin, L.A. Sands, I. Karapanou, B. Bradley, and K.J. Ressler Fear extinction in traumatized civilians with posttraumatic stress disorder: relationship to symptom severity Biol. Psychiatry 69 6 2011 556 563
67. S.P. Orr, L.J. Metzger, N.B. Lasko, M.L. Macklin, T. Peri, and R.K. Pitman De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder J. Abnorm. Psychol. 109 2 2000 290 298
68. D. Pare, G.J. Quirk, and J.E. Ledoux New vistas on amygdala networks in conditioned fear J. Neurophysiol. 92 2004 1 9
69. T. Peri, G. Ben-Shakhar, S.P. Orr, and A.Y. Shalev Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder Biol. Psychiatry 47 6 2000 512 519
70. J.E. Ploski, K.W. Park, J. Ping, M.S. Monsey, and G.E. Schafe Identification of plasticity-associated genes regulated by Pavlovian fear conditioning in the lateral amygdala J. Neurochem. 112 3 2010 636 650
71. C.A. Ponder, C.P. Huded, M.B. Munoz, F.O. Gulden, T.C. Gilliam, and A.A. Palmer Rapid selection response for contextual fear conditioning in a cross between C57BL/6J and A/J: behavioral, QTL and gene expression analysis Behav. Genet. 38 3 2008 277 291
72. C.A. Ponder, C.L. Kliethermes, M.R. Drew, J. Muller, K. Das, V.B. Risbrough, J.C. Crabbe, T.C. Gilliam, and A.A. Palmer Selection for contextual fear conditioning affects anxiety-like behaviors and gene expression Genes Brain Behav. 6 8 2007 736 749
73. C.A. Ponder, M. Munoz, T.C. Gilliam, and A.A. Palmer Genetic architecture of fear conditioning in chromosome substitution strains: relationship to measures of innate (unlearned) anxiety-like behavior Mamm. Genome 18 4 2007 221 228
74. G.J. Quirk, J.L. Armony, and J.E. LeDoux Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala Neuron 19 1997 613 624
75. G.J. Quirk, C. Repa, and J.E. LeDoux Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat Neuron 15 1995 1029 1039
76. R.A. Radcliffe, M.V. Lowe, and J.M. Wehner Confirmation of contextual fear conditioning QTLs by short-term selection Behav. Genet. 30 3 2000 183 191
77. L.G. Reijmers, J.K. Coats, M.T. Pletcher, T. Wiltshire, L.M. Tarantino, and M. Mayford A mutant mouse with a highly specific contextual fear-conditioning deficit found in an N-ethyl-N-nitrosourea (ENU) mutagenesis screen Learn. Mem. 13 2 2006 143 149
78. L.G. Reijmers, B.L. Perkins, N. Matsuo, and M. Mayford Localization of a stable neural correlate of associative memory Science 317 5842 2007 1230 1233 Aug 31
79. R.A. Rescorla Probability of shock in the presence and absence of CS in fear conditioning J. Comp. Physiol. Psychol. 66 1 1968 1 5 Aug
80. J.C. Repa, J. Muller, J. Apergis, T.M. Desrochers, Y. Zhou, and J.E. LeDoux Two different lateral amygdala cell populations contribute to the initiation and storage of memory Nat. Neurosci. 4 2001 724 731
81. L.M. Romanski, M.C. Clugnet, F. Bordi, and J.E. LeDoux Somatosensory and auditory convergence in the lateral nucleus of the amygdala Behav. Neurosci. 107 1993 444 450
82. J.A. Rosenkranz, and A.A. Grace Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning Nature 417 2002 282 287
83. S. Rumpel, J. LeDoux, A. Zador, and R. Malinow Postsynaptic receptor trafficking underlying a form of associative learning Science 308 5718 2005 83 88
84. P. Sah, and R.F. Westbrook Behavioural neuroscience: the circuit of fear Nature 454 2008 589 590
85. G.E. Schafe, M.W. Swank, S.M. Rodrigues, J. Debiec, and V. Doyre Phosphorylation of ERK/MAP kinase is required for long-term potentiation in anatomically restricted regions of the lateral amygdala in vivo Learn. Mem. 15 2 2008 55 62
86. G.E. Schafe, C.M. Atkins, M.W. Swank, E.P. Bauer, J.D. Sweatt, and J.E. LeDoux Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning J. Neurosci. 20 21 2000 8177 8187
87. D.M. Schardt, S. Erk, C. Nüsser, M.M. Nöthen, S. Cichon, M. Rietschel, J. Treutlein, T. Goschke, and H. Walter Volition diminishes genetically mediated amygdala hyperreactivity Neuroimage 53 3 2009 943 951 2010 Nov 15, Epub Dec 5
88. C. Shi, and M. Davis Visual pathways involved in fear conditioning measured with fear-potentiated startle: behavioral and anatomic studies J. Neurosci. 21 2001 9844 9855
89. F. Sotres-Bayon, D.E. Bush, and J.E. LeDoux Acquisition of fear extinction requires activation of NR2B-containing NMDA receptors in the lateral amygdala Neuropsychopharmacology 32 2007 1929 1940
90. F. Sotres-Bayon, C.K. Cain, and J.E. LeDoux Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex Biol. Psychiatry 60 2006 329 336
91. M.B. Stein, K.L. Jang, S. Taylor, P.A. Vernon, and W.J. Livesley Genetic and environmental influences on trauma exposure and posttraumatic stress disorder symptoms: a twin study Am. J. Psych. 159 2002 1675 1681
92. C. Stoppel, A. Albrecht, H.-C. Pape, and O. Stork Genes and neurons: molecular insights to fear and anxiety Genes Brain Behav. 5 Suppl. 2 2006 34 47
93. O. Stork, and H.-C. Pape Fear memory and the amygdala: insights from a molecular perspective Cell Tissue Res. 310 2002 271 277
94. G.M. Sullivan, J. Apergis, D.E. Bush, L.R. Johnson, M. Hou, and J.E. LeDoux 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 Neurosci 128 1 2004 7 14
95. W.J. True, J. Rice, S.A. Eisen, A.C. Heath, J. Goldberg, and M.J. Lyons A twin study of genetic and environmental contributions to liability for posttraumatic stress symptoms Arch. Gen. Psychiatry 50 1993 257 264
96. R.J. Ursano, L. Zhang, H. Li, L. Johnson, J. Carlton, C.S. Fullerton, and D.M. Benedek PTSD and traumatic stress from gene to community and bench to bedside Brain Res. 1293 2009 2 12
97. D.L. Walker, and M. Davis The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction Pharmacol. Biochem. Behav. 71 2002 379 392
98. S.H. Wang, L. de Oliveira Alvares, and K. Nader Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation Nat. Neurosci. 12 7 2009 905 912
99. J.M. Wehner, R.A. Radcliffe, S.T. Rosmann, S.C. Christensen, D.L. Rasmussen, D.W. Fulker, and M. Wiles Quantitative trait locus analysis of contextual fear conditioning in mice Nat. Genet. 17 3 1997 331 334
100. C.L. Wellman, A. Izquierdo, J.E. Garrett, K.P. Martin, J. Carroll, R. Millstein, K.P. Lesch, D.L. Murphy, and A. Holmes Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice J. Neurosci. 27 3 2007 684 691
101. X.H. Zhang, L.J. Wu, B. Gong, M. Ren, B.M. Li, and M. Zhuo Induction- and conditioning-protocol dependent involvement of NR2B-containing NMDA receptors in synaptic potentiation and contextual fear memory in the hippocampal CA1 region of rats Mol. Brain 1 1 2008 9