Objective: In the neocortex of rodents, excitatory, glutamatergic synapses are established during the first four weeks after birth. During this period profound changes of synaptic transmission occur which significantly change the computational properties of neurons. Methods: Intrinsic firing properties and unitary EPSPs were recorded from single and synaptically coupled layer 4 (L4) spiny neurons in 'barrel' cortex slices of rats aged 4 to 28 days (P4-P28) using whole-cell patch clamp and simultaneous biocytin fillings. Histochemical processing and subsequent 3D reconstructions were performed to reveal structural changes during development. Results: During early postnatal development, action potentials (AP) in L4 spiny neurons are characterised by a small amplitude (56.7±8.3 mV at P4), a long half-width (2.3±0.7 ms) and low maximum firing frequencies (24.9±7.9 Hz) during a train. This changes significantly with maturation to an AP amplitude of 101.2±8.8 mV, a half-width of 0.6±0.1 ms and a maximum frequency of 45.2±12.4 Hz (at P18-P23). During this time the incidence of synaptically connected L4 spiny neurons increases from <5% to a high connectivity rate of 30% in the mature. In immature animals, synaptic transmission at L4-L4 connections shows a low reliability, which increases gradually with maturation (CV: 0.55±0.29 at P4-P6, 0.28±0.11 at P18-P23). Furthermore, in immature animals, 10 Hz stimulation results in strong paired pulse depression of EPSPs (PPR: 0.46±0.15) which changes to a weak depression at P18-P23 (PPR: 0.87±0.09). Generally, a strong paired pulse depression is associated with a high release probability. However, during early neocortical development synaptic vesicle pools are not yet fully differentiated and their replenishment may be slow, thus resulting in EPSP amplitude depression. Conclusion: During development synaptic transmission in layer 4 changes from being rare and unreliable to a highly connected network with very reliable synapses.