The intrinsic physiology of inhibitory neurons changes over auditory development

During auditory development, changes in membrane properties promote the ability of excitatory neurons in the brainstem to code aspects of sound, including the level and timing of a stimulus. Some of these changes coincide with hearing onset, suggesting that sound-driven neural activity produces developmental plasticity of ion channel expression. While it is known that the coding properties of excitatory neurons are modulated by inhibition in the mature system, it is unknown whether there are also developmental changes in the membrane properties of brainstem inhibitory neurons. We investigated the primary source of inhibition in the avian auditory brainstem, the superior olivary nucleus (SON). The present studies test the hypothesis that, as in excitatory neurons, the membrane properties of these inhibitory neurons change following hearing onset. We examined SON neurons at different stages of auditory development: embryonic days 14-16 (E14-16), a time at which cochlear ganglion neurons are just beginning to respond to sound, later embryonic stages (E18-19), and after hatching (P0-P2). We used in vitro whole-cell patch electrophysiology to explore physiological changes in SON. Age-related changes were observed at the level of a single spike and in multi-spiking behavior. In particular, tonic behavior, measured as a neuron's ability to sustain tonic firing over a range of current steps, became more common later in development. Voltage-clamp recordings and biophysical models were employed to examine how age-related increases in ion currents enhance excitability in SON. Our findings suggest that concurrent increases in sodium and potassium currents underlie the emergence of tonic behavior.

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