Miniature EPSCs in the lateral superior olive before hearing onset: regional and cell-type-specific differences and heterogeneous neuromodulatory effects of ATP.

Spontaneous activity occurs in the mammalian auditory system prior to hearing onset and is relevant for neuronal differentiation. Growing evidence indicates that miniature events, i.e., action potential-independent synaptic activity, also have some developmental relevance. An intriguing question is whether these events are purely stochastic or rather display specific characteristics. We addressed this question and studied miniature excitatory postsynaptic currents (mEPSCs) in morphologically defined neurons of the rat lateral superior olive (LSO) during early neonatal life. To do so, whole-cell recordings from neurons in acute slices were combined with Lucifer yellow fillings. mEPSCs were identified by their TTX insensitivity and their blockade by glutamate receptor antagonists. Altogether, 60% of the LSO neurons displayed mEPSCs, and their presence correlated with the cell location and morphology. Their percentage was highest in the medial limb (86%) and lowest in the lateral limb (14%). Seventy-seven percent of the neurons with mEPSCs were bipolar cells, whereas 77% of those without mEPSCs were multipolar cells. The neuromodulator ATP affected the frequency of mEPSCs in 61% of the LSO neurons in a heterogeneous manner: both frequency increases and decreases occurred. These data provide further evidence for the specificity of mEPSCs. Finally, we investigated whether missing cochlear input changes mEPSCs characteristics. Characterizing LSO neurons of CaV1.3-/- mice, which lack cochlea-driven nerve activity, we observed higher mEPSC frequencies and peak amplitudes, indicative of a compensatory response to deprivation. Together, our results demonstrate specific, rather than stochastic, characteristics of mEPSCs in the neonatal LSO, in accordance with their potential developmental significance.