Retinal ganglion cells (RGCs) summate inputs across their receptive fields and forward a corresponding spike train code to the brain. Considering the many visual aspects carried by this code the comprehension of RGC firing kinetics and the underlying mechanisms is markedly important. RGCs can generate a maintained spiking (sustained) or a quickly decaying brief burst of spikes (transient) upon ON- and/or OFF-set of prolonged light stimuli. Our results here challenge the classical view that claims an outer retinal origin for RGC response transience and explains the observed response dichotomy with the dissimilar glutamate receptor kinetics in postsynaptic bipolar cell dendritic surfaces. We find that activation of the same glutamate receptor subtype can result in transient, sustained, and intermediate RGC responses. Moreover, even signaling via a single bipolar cell subtype can result in RGC responses with a variety of transience values. Contrary, a change in the dominance of inputs delivered by converging retinal pathways can alter RGC response transience considerably. Such response component fine-tuning occurs via inner retinal GABAergic inhibitory and gap junction mediated excitatory interactions. The above data thus indicate that RGC light response temporal characteristics are determined by inner retinal microcircuits and fine-tuned in a context dependent manner.