I used whole-cell voltage clamp and current clamp recordings in acute mouse olfactory bulb slices. I first demonstrate that a population of juxtaglomerular interneurons, which release both dopamine and GABA, can effectively inhibit transmitter release from primary afferent neurons, thereby potently controlling the strength of afferent input. Using single glomerular afferent stimulation, I further demonstrate that the afferent olfactory receptor nerve terminal has an extraordinarily high release probability, which is mediated by a single pool of slowly recycling vesicles. Furthermore, although mitral cells and external tufted cells receive homogenous afferent input with respect to quantal amplitudes and release probabilities, the postsynaptic processing of brief afferent input differs widely between cell types. Compared to external tufted cells, mitral cells showed robust dendrodendritic amplification of afferent input, significantly prolonging the EPSC and increasing the total synaptic charge. This amplification allowed mitral cells to respond to high frequency afferent stimulation with sustained spiking responses, despite robust synaptic depression of axodendritic input. External tufted cells, on the other hand, despite larger monosynaptic EPSCs, responded to high frequency stimulation with transient responses. This work provides important insight into the divergent synaptic processing of common olfactory input, and defines the synaptic mechanisms underlying parallel processing of afferent input.