Circuits That Innervate Excitatory-Inhibitory Cells in the Inferior Colliculus Obtained with In Vivo Whole Cell Recordings

Abstract

Neurons excited by stimulation of one ear and suppressed by the other, called excitatory/inhibitory (EI) neurons, are sensitive to interaural intensity disparities, the cues animals use to localize high frequencies. EI neurons are first formed in lateral superior olive, which then sends excitatory projections to the dorsal nucleus of the lateral lemniscus and the inferior colliculus (IC), both of which contain large populations of EI cells. We evaluate herein the inputs that innervate EI cells in the IC of Mexican free-tailed bats (Tadarida brasilensis mexicana) with in vivo whole-cell recordings from which we derived excitatory and inhibitory conductances. We show that the basic EI property in the majority of IC cells is inherited from lateral superior olive, but that each type of EI cell is also innervated by the ipsilateral or contralateral dorsal nucleus of the lateral lemniscus, as well as additional excitatory and inhibitory inputs from monaural nuclei. We identify three EI types, each of which receives a set of projections that is different from the other types. To evaluate the role that the various projections played in generating binaural responses, we used modeling to compute a predicted response from the conductances. We then omitted one of the conductances from the computation to evaluate the degree to which that input contributed to the binaural response. We show that the formation of the EI property in the various types is complex, and that some projections exert such subtle influences that they could not have been detected with extracellular recordings or even from intracellular recordings of postsynaptic potentials.