Genetic reprogramming techniques have been used with increasing success to generate human neurons from adult somatic cells. Induced pluripotent stem cell (iPSC) derived neurons have been shown as an effective way to investigate normal and pathological neuronal development. Additionally, transcription factor-based direct conversion of fibroblasts into induced neurons (iNs) has been established. Such iNs have been shown to retain age-related epigenetic information of the donor and therefore are viewed as a more appropriate model system for studying human neuronal aging and related pathologies. In our present study we aimed to compare functional properties of neurons obtained either by iPSC differentiation or by direct conversion. We performed whole-cell patch clamp measurements to evaluate the passive and active membrane parameters of neurons, to characterize their functional maturation and diversity. We found that iPSC-derived neurons exhibited relatively homogeneous cellular properties characteristic of embryonic neurons. Isogenic iNs, on the other hand, were more resembling to well differentiated neurons of adult brain circuits and exhibited signatures of various voltage-dependent currents. Next, we developed and tested an optogenetics based technique to induce activity-dependent homeostatic adaptations in the developing neuron populations. Here, we elicited firing of ChR2-transduced neurons using optical stimulation for durations of up to 48 hours. We found that such trained neurons exhibited more mature physiological properties, higher degree of intrinsic excitability than their dark-kept controls. Our findings show that activity- and pattern-dependent regulation of the physiological properties of neurons can play a significant role in shaping their mature integrative properties.