Intracellular recordings reveal novel features of neurons that code interaural intensity disparities in the inferior colliculus.

Many cells in the inferior colliculus (IC) are excited by contralateral and inhibited by ipsilateral stimulation and are thought to be important for sound localization. These excitatory-inhibitory (EI) cells comprise a diverse group, even though they exhibit a common binaural response property. Previous extracellular studies showed the diversity results from different circuits that generate the same EI property among the IC population, where some inherit the property from a lower nucleus, some are formed de novo in the IC, and others inherit EI features that are modified by inhibitory circuits. Here we evaluated the differential circuitry by recording inputs (postsynaptic potentials) and outputs (spikes) with in vivo whole-cell recordings from the IC of awake Mexican free-tailed bats. We show that in a minority of EI cells, either they inherited their binaural property from a lower binaural nucleus or the EI property was created in the IC via inhibitory projections from the ipsilateral ear, features consistent with those observed in extracellular studies. However, in a majority of EI cells, ipsilateral signals evoked subthreshold EPSPs that behaved paradoxically in that EPSP amplitudes increased with intensity, even though binaural signals with the same ipsilateral intensities generated progressively greater spike suppressions. We propose circuitry that can account for the responses we observed and suggest that the ipsilaterally evoked EPSPs could influence the responsiveness of IC cells to dynamic signals with interaural intensity disparities that change over time, such as moving sound sources or multiple sounds that occur in complex acoustic environments.