Home LiteratureArticle Details
PMID: 17264839 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories.

Molecular psychiatry ·Vol. 12 ·No. 7 ·2007-07-00 ·Pages 656-70

Heldt SA, Stanek L, Chhatwal JP, Ressler KJ

Abstract

Brain-derived neurotrophic factor (BDNF) is known to play a critical role in the synaptic plasticity underlying the acquisition and/or consolidation of certain forms of memory. Additionally, a role has been suggested for neurotrophin function within the hippocampus in protection from anxiety and depressive disorders. Understanding the function of this important gene in adult animals has been limited however, because standard knockouts are confounded by gene effects during development. There are no BDNF receptor-specific pharmacological agents, and infusions of neuropeptides or antibodies have other significant limitations. In these studies, we injected a lentivirus expressing Cre recombinase bilaterally into the dorsal hippocampus in adult mice floxed at the BDNF locus to facilitate the site-specific deletion of the BDNF gene in adult animals. Significant decreases in BDNF mRNA expression are demonstrated in the hippocampi of lenti-Cre-infected animals compared with control lenti-GFP-infected animals. Behaviorally, there were no significant effects of BDNF deletion on locomotion or baseline anxiety measured with startle. In contrast, hippocampal-specific BDNF deletions impair novel object recognition and spatial learning as demonstrated with the Morris water maze. Although there were no effects on the acquisition or expression fear, animals with BDNF deletions show significantly reduced extinction of conditioned fear as measured both with fear-potentiated startle and freezing. These data suggest that the cognitive deficits and impairment in extinction of aversive memory found in depression and anxiety disorders may be directly related to decreased hippocampal BDNF.

MeSH Terms
Animals Avoidance Learning/physiology Brain-Derived Neurotrophic Factor/genetics,metabolism Extinction, Psychological/physiology Fear/physiology Gene Deletion Gene Targeting Hippocampus/metabolism,physiopathology Male Maze Learning/physiology Mice Mice, Knockout Mice, Transgenic RNA, Messenger/analysis Recognition, Psychology/physiology Reflex, Startle/physiology Spatial Behavior/physiology
Chemicals
Brain-Derived Neurotrophic Factor RNA, Messenger
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Heldt S A
Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, USA.
Stanek L
Chhatwal J P
Ressler K J
References (86)
86 references, click to expand
  1. Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation.
    J Neurosci. 1999 Sep 15;19(18):7983-90 PMID: 10479698
  2. Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning.
    Cogn Affect Behav Neurosci. 2004 Sep;4(3):317-25 PMID: 15535167
  3. Neuroplasticity: from MRI to depressive symptoms.
    Eur Neuropsychopharmacol. 2004 Dec;14 Suppl 5:S503-10 PMID: 15550349
  4. Differential regulation of brain-derived neurotrophic factor transcripts during the consolidation of fear learning.
    Learn Mem. 2004 Nov-Dec;11(6):727-31 PMID: 15537738
  5. Regulation of gephyrin and GABAA receptor binding within the amygdala after fear acquisition and extinction.
    J Neurosci. 2005 Jan 12;25(2):502-6 PMID: 15647495
  6. The role of hippocampal subregions in detecting spatial novelty.
    Behav Neurosci. 2005 Feb;119(1):145-53 PMID: 15727520
  7. Olfactory-mediated fear conditioning in mice: simultaneous measurements of fear-potentiated startle and freezing.
    Behav Neurosci. 2005 Feb;119(1):329-35 PMID: 15727538
  8. Extinction and reacquisition of a fear-motivated memory require activity of the Src family of tyrosine kinases in the CA1 region of the hippocampus.
    Pharmacol Biochem Behav. 2005 May;81(1):139-45 PMID: 15894071
  9. 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. 2005 Jun;35(6):791-806 PMID: 15997600
  10. Reinstatement of conditioned fear in humans is context dependent and impaired in amnesia.
    Behav Neurosci. 2005 Jun;119(3):677-86 PMID: 15998188
  11. Differential contributions of hippocampus, amygdala and perirhinal cortex to recognition of novel objects, contextual stimuli and stimulus relationships.
    Brain Res Bull. 2005 Sep 30;67(1-2):62-76 PMID: 16140164
  12. Behavioral characteristics of rats predisposed to learned helplessness: reduced reward sensitivity, increased novelty seeking, and persistent fear memories.
    Behav Brain Res. 2005 Nov 7;164(2):222-30 PMID: 16095730
  13. Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction.
    J Neurosci. 2005 Sep 28;25(39):8978-87 PMID: 16192388
  14. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice.
    Circulation. 2005 Oct 25;112(17):2668-76 PMID: 16230485
  15. Emotional learning and glutamate: translational perspectives.
    CNS Spectr. 2005 Oct;10(10):831-9 PMID: 16400246
  16. Pattern of impaired working memory during major depression.
    J Affect Disord. 2006 Feb;90(2-3):149-61 PMID: 16364451
  17. Lesions of the habenula produce stress- and dopamine-dependent alterations in prepulse inhibition and locomotion.
    Brain Res. 2006 Feb 16;1073-1074:229-39 PMID: 16442084
  18. Subtle neurologic compromise as a vulnerability factor for combat-related posttraumatic stress disorder: results of a twin study.
    Arch Gen Psychiatry. 2006 May;63(5):571-6 PMID: 16651514
  19. Context fear learning in the absence of the hippocampus.
    J Neurosci. 2006 May 17;26(20):5484-91 PMID: 16707800
  20. Fear extinction in rats: implications for human brain imaging and anxiety disorders.
    Biol Psychol. 2006 Jul;73(1):61-71 PMID: 16476517
  21. A neurotrophic model for stress-related mood disorders.
    Biol Psychiatry. 2006 Jun 15;59(12):1116-27 PMID: 16631126
  22. Amygdala BDNF signaling is required for consolidation but not encoding of extinction.
    Nat Neurosci. 2006 Jul;9(7):870-2 PMID: 16783370
  23. Selective modification of short-term hippocampal synaptic plasticity and impaired memory extinction in mice with a congenitally reduced hippocampal commissure.
    J Neurosci. 2002 Sep 15;22(18):8277-86 PMID: 12223582
  24. Inhibition of mRNA and protein synthesis in the CA1 region of the dorsal hippocampus blocks reinstallment of an extinguished conditioned fear response.
    J Neurosci. 2003 Feb 1;23(3):737-41 PMID: 12574401
  25. A general method for gene knockdown in mice by using lentiviral vectors expressing small interfering RNA.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1844-8 PMID: 12552109
  26. The place of the hippocampus in fear conditioning.
    Eur J Pharmacol. 2003 Feb 28;463(1-3):217-23 PMID: 12600712
  27. The role of NMDA glutamate receptors, PKA, MAPK, and CAMKII in the hippocampus in extinction of conditioned fear.
    Hippocampus. 2003;13(1):53-8 PMID: 12625457
  28. Memory extinction requires gene expression in rat hippocampus.
    Neurobiol Learn Mem. 2003 May;79(3):199-203 PMID: 12676518
  29. Effects of chronic exercise and imipramine on mRNA for BDNF after olfactory bulbectomy in rat.
    Brain Res. 2003 Jun 6;974(1-2):228-35 PMID: 12742641
  30. Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor.
    Nat Neurosci. 2003 Jul;6(7):736-42 PMID: 12796784
  31. Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder.
    Biol Psychiatry. 2003 Oct 1;54(7):693-702 PMID: 14512209
  32. Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice.
    Neuroscience. 2003;121(2):341-54 PMID: 14521993
  33. Functional neuroanatomical correlates of traumatic stress revisited 7 years later, this time with data.
    Psychopharmacol Bull. 2003 Spring;37(2):6-25 PMID: 14566211
  34. Brain-derived neurotrophic factor mRNA downregulation produced by social isolation is blocked by intrahippocampal interleukin-1 receptor antagonist.
    Neuroscience. 2003;121(4):847-53 PMID: 14580934
  35. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor.
    Neuroscience. 2004;123(2):429-40 PMID: 14698750
  36. Distinct roles of hippocampal de novo protein synthesis and actin rearrangement in extinction of contextual fear.
    J Neurosci. 2004 Feb 25;24(8):1962-6 PMID: 14985438
  37. Applying learning principles to the treatment of post-trauma reactions.
    Ann N Y Acad Sci. 2003 Dec;1008:112-21 PMID: 14998877
  38. On the delay-dependent involvement of the hippocampus in object recognition memory.
    Neurobiol Learn Mem. 2004 Jul;82(1):26-34 PMID: 15183168
  39. Essential role of brain-derived neurotrophic factor in adult hippocampal function.
    Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10827-32 PMID: 15249684
  40. Brain-derived neurotrophic factor plays a critical role in contextual fear conditioning.
    J Neurosci. 2004 Sep 8;24(36):7958-63 PMID: 15356210
  41. Discovering endophenotypes for major depression.
    Neuropsychopharmacology. 2004 Oct;29(10):1765-81 PMID: 15213704
  42. Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice.
    Brain Res. 2004 Oct 29;1025(1-2):10-20 PMID: 15464739
  43. Context and behavioral processes in extinction.
    Learn Mem. 2004 Sep-Oct;11(5):485-94 PMID: 15466298
  44. Crouching as an index of fear.
    J Comp Physiol Psychol. 1969 Mar;67(3):370-5 PMID: 5787388
  45. Passive and active reactions to fear-eliciting stimuli.
    J Comp Physiol Psychol. 1969 May;68(1):129-35 PMID: 5793861
  46. Place navigation impaired in rats with hippocampal lesions.
    Nature. 1982 Jun 24;297(5868):681-3 PMID: 7088155
  47. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data.
    Behav Brain Res. 1988 Nov 1;31(1):47-59 PMID: 3228475
  48. Effects of amygdaloid and amygdaloid-hippocampal lesions on object recognition and spatial working memory in rats.
    Behav Neurosci. 1989 Oct;103(5):962-74 PMID: 2803563
  49. The role of the amygdala in fear and anxiety.
    Annu Rev Neurosci. 1992;15:353-75 PMID: 1575447
  50. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus.
    J Neurosci. 1995 Mar;15(3 Pt 1):1768-77 PMID: 7891134
  51. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder.
    Am J Psychiatry. 1995 Jul;152(7):973-81 PMID: 7793467
  52. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8856-60 PMID: 7568031
  53. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments.
    J Neurosci. 1995 Nov;15(11):7539-47 PMID: 7472505
  54. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11382-8 PMID: 8876144
  55. Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat.
    Behav Brain Res. 1996 Oct;80(1-2):9-25 PMID: 8905124
  56. Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task.
    Behav Neurosci. 1997 Feb;111(1):104-13 PMID: 9109628
  57. Essential role for TrkB receptors in hippocampus-mediated learning.
    Neuron. 1999 Oct;24(2):401-14 PMID: 10571233
  58. Hippocampal volume reduction in major depression.
    Am J Psychiatry. 2000 Jan;157(1):115-8 PMID: 10618023
  59. Is the hippocampus necessary for contextual fear conditioning?
    Behav Brain Res. 2000 Jun 1;110(1-2):83-95 PMID: 10802306
  60. The hippocampus and contextual memory retrieval in Pavlovian conditioning.
    Behav Brain Res. 2000 Jun 1;110(1-2):97-108 PMID: 10802307
  61. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning.
    Nat Neurosci. 2000 Jun;3(6):533-5 PMID: 10816306
  62. The effects of neurotoxic hippocampal lesions on two effects of context after fear extinction.
    Behav Neurosci. 2000 Apr;114(2):227-40 PMID: 10832785
  63. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats.
    J Neurosci. 2000 Sep 15;20(18):7116-21 PMID: 10995859
  64. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction.
    J Neurosci. 2001 Mar 1;21(5):1720-6 PMID: 11222661
  65. Hippocampus and contextual fear conditioning: recent controversies and advances.
    Hippocampus. 2001;11(1):8-17 PMID: 11261775
  66. Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear.
    J Neurosci. 2001 Aug 1;21(15):5773-80 PMID: 11466449
  67. Applications of the Morris water maze in the study of learning and memory.
    Brain Res Brain Res Rev. 2001 Aug;36(1):60-90 PMID: 11516773
  68. Delivery of the Cre recombinase by a self-deleting lentiviral vector: efficient gene targeting in vivo.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11450-5 PMID: 11553794
  69. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity.
    Mol Endocrinol. 2001 Oct;15(10):1748-57 PMID: 11579207
  70. Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus.
    Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):12251-4 PMID: 11572949
  71. When cells become depressed: focus on neural stem cells in novel treatment strategies against depression.
    J Neural Transm (Vienna). 2002 May;109(5-6):947-62 PMID: 12111481
  72. Neuroimaging studies in post-traumatic stress disorder.
    Curr Psychiatry Rep. 2002 Aug;4(4):254-63 PMID: 12126593
  73. Regulation of synaptic plasticity genes during consolidation of fear conditioning.
    J Neurosci. 2002 Sep 15;22(18):7892-902 PMID: 12223542
  74. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
    Behav Neurosci. 1992 Apr;106(2):274-85 PMID: 1590953
  75. Mice lacking brain-derived neurotrophic factor develop with sensory deficits.
    Nature. 1994 Mar 10;368(6467):147-50 PMID: 8139657
  76. A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice.
    Horm Behav. 1997 Jun;31(3):197-211 PMID: 9213134
  77. A molecular and cellular theory of depression.
    Arch Gen Psychiatry. 1997 Jul;54(7):597-606 PMID: 9236543
  78. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies.
    Psychopharmacology (Berl). 1997 Jul;132(2):107-24 PMID: 9266608
  79. Evidence of contextual fear after lesions of the hippocampus: a disruption of freezing but not fear-potentiated startle.
    J Neurosci. 1997 Dec 1;17(23):9353-60 PMID: 9364080
  80. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats.
    Behav Brain Res. 1997 Nov;88(2):261-74 PMID: 9404635
  81. The hippocampus, objects, and their contexts.
    Behav Neurosci. 1997 Dec;111(6):1228-44 PMID: 9438792
  82. Learning deficit in BDNF mutant mice.
    Eur J Neurosci. 1997 Dec;9(12):2581-7 PMID: 9517463
  83. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning.
    Behav Neurosci. 1998 Aug;112(4):863-74 PMID: 9733192
  84. Learning upregulates brain-derived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance?
    Behav Neurosci. 1998 Aug;112(4):1012-9 PMID: 9733207
  85. Development of a self-inactivating lentivirus vector.
    J Virol. 1998 Oct;72(10):8150-7 PMID: 9733856
  86. Generalized lacZ expression with the ROSA26 Cre reporter strain.
    Nat Genet. 1999 Jan;21(1):70-1 PMID: 9916792
Article Info
Journal
Molecular psychiatry
Abbr.
Mol Psychiatry
ISSN
1359-4184
Published
2007-07-00
Epub
2007-00-30
Pages
656-70
Language
English
Region
England
NLM ID
9607835
PMCID
PMC2442923
Subset
IM
Grants
NIGMS NIH HHS · T32 GM008169 · United States
NIMH NIH HHS · MH069884 · United States
NCRR NIH HHS · P51 RR000165 · United States
NIDA NIH HHS · R01 DA019624-01A2 · United States
NIMH NIH HHS · K01 MH069884 · United States
NCRR NIH HHS · P51RR000165 · United States
NIDA NIH HHS · R01 DA019624 · United States
NIMH NIH HHS · F30 MH070218 · United States
NIMH NIH HHS · MH070218 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com