In the mature cochlea, inner hair cells (IHCs) signal the reception of sound by means of graded receptor potentials with rapid kinetics. Before the onset of hearing, which occurs at about postnatal day 12 in small altricial rodents such as mice, rats and gerbils, the IHCs fire spontaneous action potentials with mean frequencies in the order of one Hz instead (Kros et al 1998; Johnson et al 2011). Developmental changes in ion channel expression along the basolateral membrane of the IHCs, mainly the replacement of a slow delayed-rectifier potassium current, IK,neo, with a fast BK current, IK,f and changes in the Ca2+-dependence of neurotransmitter release, underlie this switch in function (reviewed by Kros 2007). Speculation about the possible roles for these spontaneous action potentials includes that they may be important for the correct maturation of the IHCs and their innervation, which undergoes considerable change between birth and the onset of hearing. Another potential function is that spontaneous activity may be required for the refinement of tonotopic maps to enable frequency analysis, in the IHCs themselves or further along the auditory pathway. A number of recent findings is beginning to provide some evidence. The action potential pattern is found to vary as a function of location of the IHCs along the cochlea, so that immature apical IHCs fire action potentials in bursts, whereas basal IHC fire more randomly (Johnson et al 2011). Within the bursts of the apical IHCs the frequency of the action potentials is similar to that of the randomly firing action potentials in the base, but the overall mean frequency is lower in the apex. This might in principle serve as a signal that could be used to set up a tonotopic gradient. The bursts in the apical-coil IHCs depend on release of acetylcholine (ACh) by the efferent terminals hyperpolarizing the IHCs via SK2 channels closely coupled to the ACh receptors, whereas the firing of the basal-coil IHCs depends on hyperpolarization by ATP, again via SK2 channels coupled to P2X receptors (Johnson et al 2011). ATP is released in waves in the immature postnatal cochlea from supporting cells situated to the modiolar side of the IHCs (Tritsch et al 2007). Another useful finding is that, at least in the second postnatal week, action potential firing is inferred to depend on the mechano-electrical transducer current that flows when the hair bundle is at rest (Johnson et al 2012), i.e. in the absence of sound stimulation (which does not reach the inner ear yet at this stage of development). This may explain why IHCs of mice with mutations that affect the function of proteins in the mechanosensitive hair bundle, such as myosin 6 and myosin 7a, fail to mature into fully functional auditory hair cells (myosin 6: Roux et al 2009; myosin 7a: Roberts, Ranatunga and Kros in preparation). The absence of a resting transducer current might prevent action potential activity in these cases, leading to a failure of maturation of the IHCs. Challenging questions remain. For example, what causes the developmental failure of outer hair cells (OHCs), which in the myosin 7a mutants fail to express their characteristic KCNQ4 potassium current IK,n (Roberts, Ranatunga and Kros in preparation)? OHCs are not generally thought to fire spontaneous action potentials during development. Would this developmental programme have to be repeated if fully functional mature hair cells are to be regenerated in the mammalian cochlea? Since spiral ganglion cells already exhibit intrinsic spontaneous activity at embryonic day 14 (E14) in mice (Marrs and Spirou 2012), well before that of the IHCs starts at E17.5 in the base and E18.5 in the apex, it would be interesting to investigate their respective roles in the functional maturation of the auditory pathway.