The Ca(2+) current (I(Ca)) in prehearing and adult inner hair cells (IHCs), the primary sensory receptors of the mammalian cochlea, is mainly carried by L-type (Ca(V)1.3) Ca(2+) channels. I(Ca) in immature and adult IHCs triggers the release of neurotransmitter onto auditory afferent fibres in response to spontaneous action potentials (APs) or graded receptor potentials, respectively. We have investigated whether the biophysical properties of I(Ca) vary between low- and high-frequency IHCs during cochlear development and whether its inactivation influences cellular responses. I(Ca) was recorded from gerbil IHCs maintained near physiological recording conditions. The size of I(Ca) in adult IHCs was about a third of that in immature cells with no apparent difference along the cochlea at both stages. The activation kinetics of I(Ca) were significantly faster in high-frequency IHCs, with that of adult cells being more rapid than immature cells. The degree of I(Ca) inactivation was similar along the immature cochlea but larger in high- than low-frequency adult IHCs. This inactivation was greatly reduced with barium but not affected by changing the intracellular buffer (BAPTA instead of EGTA). Immature basal IHCs showed faster recovery of I(Ca) from inactivation than apical cells allowing them to support a higher AP frequency. I(Ca) in adult IHCs was more resistant to progressive inactivation following repeated voltage stimulation than that of immature cells. This suggests that adult IHCs are likely to be suited for sustaining rapid and repeated release of synaptic vesicles, which is essential for sound encoding.