A　human　variant　in　the　BDNF　gene　(Val66Met;　rs6265)　is　associated　with　impaired　fear　extinction.　Using　super-resolution　imaging,　we　demonstrate　that　the　BDNF　Met　prodomain　disassembles　dendritic　spines　and　eliminates　synapses　in　hippocampal　neurons.　In　vivo,　ventral　CA1　(vCA1)　hippocampal　neurons　undergo　similar　morphological　changes　dependent　on　their　transient　co-expression　of　a　SorCS2/p75(NTR)　receptor　complex　during　peri-adolescence.　BDNF　Met　prodomain　infusion　into　the　vCA1　during　this　developmental　time　frame　reduces　dendritic　spine　density　and　prelimbic　(PL)　projections,　impairing　cued　fear　extinction.　Adolescent　Bdnf(Met/Met)　mice　display　similar　spine　and　PL　innervation　deficits.　Using　fiber　photometry,　we　found　that,　in　wild-type　mice,　vCA1　neurons　projecting　to　the　PL　encode　extinction　by　enhancing　neural　activity　in　threat　anticipation　and　rapidly　subsiding　their　response.　This　adaptation　is　absent　in　BDNFMet/Met　mice.　We　conclude　that　the　BDNF　Met　prodomain　renders　vCA1-PL　projection　neurons　underdeveloped,　preventing　their　capacity　for　subsequent　circuit　modulation　necessary　for　fear　extinction.