TrkB modulates fear learning and amygdalar synaptic plasticity by specific docking sites

Journal of Neuroscience

Volumn 29, Issue 32, 2009, Pages 10131-10143

  Musumeci, Gabriele ^a   Sciarretta, Carla ^a,g   Rodríguez Moreno, Antonio ^b   Al Banchaabouchi, Mumna ^a   Negrete Díaz, Vicente ^b   Costanzi, Marco ^c   Berno, Valeria ^a   Egorov, Alexei V ^d   Von Bohlen Und Halbach, Oliver ^d,h   Cestari, Vincenzo ^c,e   Delgado García, José M ^b   Minichiello, Liliana ^a,f  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^b UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^c CNR   (Italy)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e LUMSA UNIVERSITY   (Italy)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g ACTELION PHARMACEUTICALS LTD   (Switzerland)

^h UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; DOCKING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE B;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; FEAR; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NEUROBIOLOGY; NOCICEPTION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STATE DEPENDENT LEARNING; SYNAPTIC TRANSMISSION;

AMYGDALA; ANIMALS; BINDING SITES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CONDITIONING, CLASSICAL; FEAR; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MAZE LEARNING; MEMBRANE GLYCOPROTEINS; MEMORY; MICE; MICE, MUTANT STRAINS; NEURONAL PLASTICITY; PHOSPHORYLATION; POINT MUTATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 68849094397     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1707-09.2009     Document Type: Article

References (40)

1. Blum R, Konnerth A (2005) Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology 20:70-78.
2. Campeau S, Davis M (1995) 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 15:2312-2327.
3. Davis M (1997) Neurobiology of fear responses: the role of the amygdala. J Neuropsychiatry Clin Neurosci 9:382-402.
4. Everitt BJ, Cardinal RN, Parkinson JA, Robbins TW (2003) Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning. Ann N Y Acad Sci 985:233-250.
5. Fendt M, Fanselow MS (1999) The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 23:743-760.
6. Finkbeiner S, Tavazoie SF, Maloratsky A, Jacobs KM, Harris KM, Greenberg ME (1997) CREB: a major mediator of neuronal neurotrophin responses. Neuron 19:1031-1047.
7. Gale GD, Anagnostaras SG, Godsil BP, Mitchell S, Nozawa T, Sage JR, Wiltgen B, Fanselow MS (2004) Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J Neurosci 24:3810-3815.
8. Gruart A, Sciarretta C, Valenzuela-Harrington M, Delgado-García JM, Minichiello L (2007) Mutation at the TrkB PLC{gamma}-docking site affects hippocampal LTP and associative learning in conscious mice. Learn Mem 14:54-62.
9. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677.
10. Koo JW, Han JS, Kim JJ (2004) Selective neurotoxic lesions of basolateral and central nuclei of the amygdale produce differential effects on fear conditioning. J Neurosci 24:7654-7662.
11. Koponen E, Võikar V, Riekki R, Saarelainen T, Rauramaa T, Rauvala H, Taira T, Castrén E (2004) Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLCgamma pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci 26:166-181.
12. Lavond DG, Kim JJ, Thompson RF (1993) Mammalian brain substrates of aversive classical conditioning. Annu Rev Psychol 44:317-342.
13. LeDoux JE (1996) The emotional brain: the mysterious underpinnings of emotional life. New York: Simon and Schuster.
14. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
15. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062-1069.
16. Lin CH, Yeh SH, Lin CH, Lu KT, Leu TH, Chang WC, Gean PW (2001) A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31:841-851.
17. Maren S (2001) Neurobiology of pavlovian fear conditioning. Annu Rev Neurosci 24:897-931.
18. Maren S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and pavlovian fear conditioning in rats. Behav Brain Res 88:261-274.
19. McKernan MG, Shinnick-Gallagher P (1997) Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390:607-611.
20. Medina DL, Sciarretta C, Calella AM, Von Bohlen Und Halbach O, Unsicker K, Minichiello L (2004) TrkB regulates neocortex formation through the Shc/PLCgamma-mediated control of neuronal migration. EMBO J 23:3803-3814.
21. Minichiello L, Casagranda F, Tatche RS, Stucky CL, Postigo A, Lewin GR, Davies AM, Klein R (1998) Point mutation in trkB causes loss of NT4-dependent neurons without major effects on diverse BDNF responses. Neuron 21:335-345.
22. Minichiello L, Korte M, Wolfer D, Kühn R, Unsicker K, Cestari V, Rossi-Arnaud C, Lipp HP, Bonhoeffer T, Klein R (1999) Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24:401-414.
23. Minichiello L, Calella AM, Medina DL, Bonhoeffer T, Klein R, Korte M (2002) Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36:121-137.
24. Miyamoto Y, Chen L, Sato M, Sokabe M, Nabeshima T, Pawson T, Sakai R, Mori N (2005) Hippocampal synaptic modulation by the phosphotyrosine adapter protein ShcC/N-Shc via interaction with the NMDA receptor. J Neurosci 25:1826-1835.
25. Nagy A, Delgado-Escueta AV (1984) Rapid preparation of synaptosomes from mammalian brain using nontoxic isoosmotic gradient material (Percoll). J Neurochem 43:1114-1123.
26. Olton DS, Walker JA, Gage FH (1978) Hippocampal connections and spatial discrimination. Brain Res 139:295-308.
27. Ou LC, Gean PW (2006) Regulation of amygdala-dependent learning by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol-3-kinase. Neuropsychopharmacology 31:287-296.
28. Paré D, Quirk GJ, Ledoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92:1-9.
29. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
30. Postigo A, Calella AM, Fritzsch B, Knipper M, Katz D, Eilers A, Schimmang T, Lewin GR, Klein R, Minichiello L (2002) Distinct requirements for TrkB and TrkC signaling in target innervation by sensory neurons. Genes Dev 16:633-645.
31. Rattiner LM, Davis M, French CT, Ressler KJ (2004) Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J Neurosci 24:4796-4806.
32. Rodrigues SM, Schafe GE, LeDoux JE (2004a) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44:75-91.
33. 2+/ calmodulin-dependent protein kinase II at lateral amygdala synapses. J Neurosci 24:3281-3288.
34. Rogan MT, Stäubli UV, LeDoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390:604-607.
35. Romanski LM, LeDoux JE (1992) Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J Neurosci 12:4501-4509.
36. Rossi-Arnaud C, Ammassari-Teule M (1998) What do comparative studies of inbread mice add to current investigations on the neural basis of spatial behaviors? Exp Brain Res 123:36-44.
37. Schafe GE, Nader K, Blair HT, LeDoux JE (2001) Memory consolidation of pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci 24:540-546.
38. Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323-331.
39. Weisskopf MG, Bauer EP, LeDoux JE (1999) L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. J Neurosci 19:10512-10519.
40. Xu B, Gottschalk W, Chow A, Wilson RI, Schnell E, Zang K, Wang D, Nicoll RA, Lu B, Reichardt LF (2000) The role of brain-derived neurotrophic factor receptors in the mature hippocampus: modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J Neurosci 20:6888-6897.