Timely reaction to salient stimuli is essential for survival. The subcortical thalamic-basolateral amygdala (BLA) pathway ensures rapid processing. Here, we show that BLA neuronal, and thalamic axonal activity mirror the defensive behaviour evoked by an innate-visual-threat as well as an auditory-learned-threat. Perturbing this pathway compromises defensive responses to both threats. Our side-by-side examination highlights innate and learned threat processing in the subcortical amygdala pathway, thus providing new fundamental insights. Next, we examined the role of homo- and hetero-synaptic plasticity in consolidating transient aversive experiences in a synapse-specific manner in the same pathway.Hebbian-plasticity, proposes that experiences are transformed into memories through input-specific synaptic plasticity at the time of learning. However, synaptic plasticity is neither input-specific nor restricted to the time of its induction. The impact of such forms of non-Hebbian plasticity on memory is poorly understood. Here, we demonstrated that synaptic manipulations can deviate from the Hebbian learning yet produce a lasting memory. First, we established a weak Pavlovian conditioning protocol where optogenetic stimulation of sensory thalamic input to the amygdala was paired with a foot-shock, but no detectable memory was formed. However, potentiating the input minutes before or up to 24 hours later, converted the associative experience into a lasting memory. Importantly, potentiating a converging cortical input to the amygdala minutes after the pairing also produced a lasting memory. Thus, our findings suggest that the transformation of a transient experience into a memory is neither restricted to the time of the experience nor to the synapses triggered by it.