The ability to generate regionally defined neuronal populations from human embryonic stem cells (hESCs) provides an important new experimental resource for the investigation of human neuronal physiology and disease. In order to realise this promise there is a need to address fundamental, unanswered questions pertaining to the ability of such hESC-derived neurones to exhibit multiple functional properties relating to the regionally defined population. In this regard, we have performed a detailed electrophysiological study of stem cell-derived neurones with a human cortical identity. H9 hESCs were neuralised in suspension using chemically defined medium. Such an approach was based upon the default model of neurogenesis that minimizes extrinsic and intrinsic signals that lead to alternative cell fates. Analysis of the resulting neural stem cells (NSCs) revealed a forebrain identity as determined by FoxG1 and Otx2 expression. NSCs that are plated as a monolayer culture subsequently generates predominantly Pax6-positive precursors that terminally differentiate into a mixed population of cortical neurones showing CTIP2, SAT2B or Reelin expression. The electrophysiological properties of neurones were sampled weekly up to Week 5 (inclusively) after plate down of neural stem cells. From Wk1 to Wk5, whole-cell capacitance measurements increased (p<0.001) from 6.5 ± 0.4 pF to 17.6 ± 1.4 pF, resting membrane potential hyperpolarizes from -43.8 ± 2.1 mV to -56.9 ± 2.1 mV (p<0.001) and the input resistance of the neurones decreased insignificantly from 2361 ± 185 MΩ to 1486 ± 101 MΩ. By Wk 5 nearly all cells patched fired TTX-sensitive action potentials in response to current input (>95%), where the majority of these responses (60%) were in the form of trains of action potentials. Correspondingly, there was a developmental increase in the current density of voltage-gated sodium and potassium channels. AMPA-, GABA- and NMDA-evoked currents were recorded from the neurones, and at Wk 5 the current densities (in pA/pF) were found to be 87.8 ± 7.5 (n = 30), 3.2 ± 0.5 (n = 30) and 1.2 ± 0.3 (n = 30) respectively. Perforated-patch-clamp experiments using gramicidin demonstrated that GABA mediated a depolarising response (n = 8) that had a reversal potential of -46.1 ± 4.0 mV (n = 5) consistent with an immature phenotype. In addition neurones also display tetrodotoxin-insensitive mEPSCs that are blocked by CNQX. Further pharmacological assessment of NMDA and AMPA-evoked currents also indicated the presence of receptor complexes associated with early-stage development. Taken together our data indicate these hESC-derived neurones possess an embryonic-like phenotype compatible with immature cortical neurons. The data suggests the protocol employed is a model of human corticogenesis in vitro.