Fate choice decision and the initiation of neuronal development occur in precursor cells of the adult dentate gyrus. We here show that the earliest signs of neuronal function can be detected in a nestin-positive progenitor cell population, which is morphologically distinct from the putative radial glia-like stem cells. Whereas radial glia-like stem cells had a glial physiological phenotype, this other cell population was more heterogeneous including cells with the ability to generate action potentials. These cells had only plump horizontal processes or lacked processes. Some of these cells received spontaneous and evoked synaptic input, which was sensitive to GABA_A, but not to glutamate receptor antagonists. In radial glia-like stem cells, such a response was not observed. However, both types of precursor cells expressed functional GABA_A and glutamate receptors and glutamate transporters. This early establishment of GABAergic innervation in adult neurogenesis thus mimics the pattern described for brain development.