Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive

Abstract

Immunostaining of the cat superior olivary complex with antisera against glycine, calbindin, GABA, and its synthetic enzyme, glutamate decarboxylase (GAD) reveals considerable new information about neural connections that underlie processing of binaural signals. Antisera against glycine and calbindin immunostain principal cells and processes of the medial nucleus of the trapezoid body (MNTB). The extent of staining of fine processes afforded by the calbindin antisera reveals collateral processes of MNTB axons within the medial superior olive (MSO) and numerous terminals of these collaterals on neuronal somata and proximal dendrites. Electron microscopic immunocytochemistry of these terminals shows them to have the morphological features characteristic of inhibitory synapses, indicating that there can be considerable inhibitory inputs to MSO cells from the contralateral cochlear nucleus via the MNTB. Immunostaining for GAD and GABA shows some GABAergic inputs, mostly to dendrites within the MSO. Within the MNTB there are elaborate GABAergic endings that surround the principal cells. Electron microscopic immunocytochemistry of these terminals reveals the expected features characteristic of inhibitory synapses. The glycinergic inhibitory output of the MNTB cells is therefore subject to disinhibition by activity of these elaborate GABAergic inputs. Other endings that immunostain with antisera to leucine- enkephalin and neurotensin are found in modest amounts in both MSO and MNTB. Immunostaining of neuronal somata within the superior olivary complex suggests that the origins of the peptidergic and GABAergic endings in the MSO and MNTB may be periolivary cells. Whatever the origins, the results clearly indicate that control of the inhibitory GABAergic inputs to the MNTB can profoundly affect the inhibitory glycinergic MNTB outputs to other principal olivary nuclei. Investigations of the circumstances under which these circuits are activated will reveal much about neural processing that underlies binaural hearing.