Distress calls of mice pups outside their nest elicit reliable pup retrieval in maternal female mice but not in their virgin (`naive') conspecifics. However, when co-housed with maternal mice, naive mice become `experienced' and learn to reliably perform pup retrieval. This process correlates with neuronal changes in the primary auditory cortex (A1): While excitatory (E) neuron responses are sharply tuned to a certain inter- pup-call interval and inhibitory (I) neuron responses are broadly tuned in naive mice, the two neuron types are co-tuned in experienced mice. This change in behavior and tuning is mediated by oxytocin (Marlin et al., 2015; Schiavo et al., 2020). Here, we aim to dissect the underlying mechanisms behind the behaviorally-relevant changes in tuning of excitatory and inhibitory neurons from naive to experienced mice by combining computational modeling and in-vitro experiments. Using optogenetic targeting of somatostatin-positive (SST) or parvalbumin-positive (PV) inhibitory neurons, we quantified short-term plasticity (STP) at SST-to-E and PV-to-E connections. Furthermore, pairing experiments reveal sufficient long-term plasticity at SST-to-E but not PV-to-E connections. Using a model, we study the interaction of three neuron populations (E, SST, and PV) with synapses experiencing experimentally-identified short- and long-term plasticity. We show that 1) short-term plasticity leads to the tuning of excitatory and inhibitory neurons to specific inter-stimulus intervals (ISIs), and 2) oxytocin-gated long-term plasticity of E-to-E and SST-to-E connections leads to experience-dependent changes in the tuning properties from naive to experienced mice. Furthermore, 3) short-term plasticity at SST-to-E and PV-to-E synapses can control the excitatory signal amplitude without changing the tuning properties. Our results reveal that short- and long-term plasticity cooperate to generate tuning of excitatory and inhibitory neurons in local microcircuits and have important implications for maternal behavior.