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The Journal of Neuroscience, August 12, 2009, 29(32):10131-10143; doi:10.1523/JNEUROSCI.1707-09.2009

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Cellular/Molecular
TrkB Modulates Fear Learning and Amygdalar Synaptic Plasticity by Specific Docking Sites

Gabriele Musumeci,1 * Carla Sciarretta,1 * Antonio Rodríguez-Moreno,2 * Mumna Al Banchaabouchi,1 Vicente Negrete-Díaz,2 Marco Costanzi,3 Valeria Berno,1 Alexei V. Egorov,4 Oliver von Bohlen und Halbach,4 Vincenzo Cestari,3,5 José M. Delgado-García,2 and Liliana Minichiello1,6

1Mouse Biology Unit, European Molecular Biology Laboratory, 00015 Monterotondo, Italy, 2División de Neurociencias, Universidad Pablo de Olavide, 41013 Sevilla, Spain, 3Istituto di Neuroscienze, Consiglio Nazionale delle Ricerche, 00143 Rome, Italy, 4Interdisciplinary Center for Neurosciences, Department of Neuroanatomy, University of Heidelberg, D-69120 Heidelberg, Germany, 5Facoltà di Scienze della Formazione, Università Lumsa, 00193 Rome, Italy, and 6Centre for Neuroregeneration, University of Edinburgh, EH16 4SB Edinburgh, United Kingdom

Correspondence should be addressed to Dr. Liliana Minichiello, EMBL Mouse Biology Unit, Via Ramarini, 32, 00015 Monterotondo, Italy. Email: minichiello{at}embl.it

Understanding the modulation of the neural circuitry of fear is clearly one of the most important aims in neurobiology. Protein phosphorylation in response to external stimuli is considered a major mechanism underlying dynamic changes in neural circuitry. TrkB (Ntrk2) neurotrophin receptor tyrosine kinase potently modulates synaptic plasticity and activates signal transduction pathways mainly through two phosphorylation sites [Y515/Shc site; Y816/PLC{gamma} (phospholipase C{gamma}) site]. To identify the molecular pathways required for fear learning and amygdalar synaptic plasticity downstream of TrkB, we used highly defined genetic mouse models carrying single point mutations at one of these two sites (Y515F or Y816F) to examine the physiological relevance of pathways activated through these sites for pavlovian fear conditioning (FC), as well as for synaptic plasticity as measured by field recordings obtained from neurons of different amygdala nuclei. We show that a Y816F point mutation impairs acquisition of FC, amygdalar synaptic plasticity, and CaMKII signaling at synapses. In contrast, a Y515F point mutation affects consolidation but not acquisition of FC to tone, and also alters AKT signaling. Thus, TrkB receptors modulate specific phases of fear learning and amygdalar synaptic plasticity through two main phosphorylation docking sites.

Received April 8, 2009; revised May 15, 2009; accepted July 6, 2009.

Correspondence should be addressed to Dr. Liliana Minichiello, EMBL Mouse Biology Unit, Via Ramarini, 32, 00015 Monterotondo, Italy. Email: minichiello{at}embl.it






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