Organization of GABAergic inhibition in the motor output layer of the superior colliculus

Abstract

The direction and amplitude of saccadic eye movements are determined by the location of the center of gravity of burst activity over a neuronal population on the spatial map of the intermediate gray layer (SGI) of the superior colliculus (SC). GABAergic interneurons might play critical roles in shaping the activation field on the topographical map but, to understand the mechanism, basic information on the organization of inhibitory circuits is essential. In the present study, we investigated the electrophysiological and morphological properties of GABAergic neurons in SGI by whole-cell patch-clamp recordings and intracellular staining using biocytin in GAD67-GFP knock-in mice (PND17-22), in which GABAergic neurons specifically express GFP fluorescence. The most common firing properties among these GABAergic neurons (n=231) were fast spiking (58%), followed by burst spiking (29%), late spiking (8%) and, the least common, regular spiking (2%) and rapid spike inactivation (3%). Morphological analysis of axonal trajectories of intracellularly-labeled GABAergic neurons revealed three major subclasses: (i) intralaminar interneurons, which were further divided into two subclasses, local and horizontal interneurons; (ii) interlaminar interneurons; and (iii) commissural and tectofugal neurons. These results reveal distinct subsets of GABAergic neurons including neurons that mediate local and long-range inhibition in the SC, neurons that potentially modulate visual and other sensory inputs to the SC, and neurons that project to nuclei outside the SC.