The consolidation of long-term potentation (LTP) in the dentate gyrus of anesthetized rats requires a sustained synthesis of activity-regulated cytoskeleton-associated protein (Arc) over a period of hours. Brief intrahippocampal infusion of brain-derived neurotrophic factor (BDNF) similarly evokes Arc-dependent enhancement of medial perforant path-evoked synaptic transmission. Here we examined the role of endogenous BDNF signaling in high-frequency stimulation (HFS)-evoked LTP. Unilateral local infusion of TrkB-Fc, an extracellular fusion protein that sequesters secreted TrkB ligands, prior to HFS inhibited LTP, blocked TrkB activation and Arc protein in dentate gyrus synaptoneurosomes prepared ex vivo. LTP was rapidly and completely reversed by infusion of TrkB-Fc at 15 min, 2 h, and 4 h (but not 8 h and 10 h) post-HFS. We studied the signaling pathways and molecular mechanisms that underlie the involvement of TrkB in LTP with precipitation assays. The activated forms phospholipase C gamma1 (PLC?1) and RasGrf1 were transiently recruited to TrkB during the early-phase of LTP while Shc was observed to be activated in the late-phase of LTP thus proving that TrkB activation during LTP leads to conjoint temporal activation of several pathways. Previous work identified a role for extracellular signal-regulated kinase (ERK) and mitogen-activated protein kinase-interacting kinase (MNK) signaling in protein translational initiation and Arc synthesis during LTP consolidation. In this study ERK-MNK signaling was found to be crucial for the sustenance of translation process in the maintenance of LTP and associated TrkB signaling. Increased translation initiation during LTP was associated with release of translation repressor cytoplasmic FMRP interacting protein (CYFIP1) from mRNA cap-binding factor 4E (eIF4E) and this was dependent on TrkB-ERK-MNK signaling.