Development of Functional Interlaminar Pathways in the Mouse Superior Colliculus Revealed by Optical Imaging with Axonal Labeling

Abstract

The superior colliculus (SC) is a laminated midbrain structure responsible for visual orientation behaviors. In the mature SC, neurons in the stratum griseum superficiale (SGS) receive visual inputs that contribute to exciting premotor neurons in the stratum griseum intermediale (SGI) through a dorsoventral pathway. SGI activation generates feedback signals to the SGS through a ventrodorsal pathway. However, the developmental changes in signal transmission within the SC around the time of eye opening are not yet well understood. We compared the functional connections between the SGS and SGI before and after eye opening by imaging the neuronal population responses using a voltage-sensitive absorption dye in mouse SC slices. Electrophoresis of a fluorescent dye from the stimulating electrodes was used to fill the cells in the stimulated site. We here show that the dorsoventral transmission is present both before and after eye opening. This is in contrast to our previous finding that the ventrodorsal transmission develops after eye opening. Functions of intrinsic inhibitory systems mediated by gamma-aminobutyric acid were also investigated with the antagonist. The processes stained by electrophoresis from stimulating electrodes before eye opening were confined within the respective stimulated layers. Whereas, after eye opening, the processes were widely extended especially dorsoventrally and ventrodorsally invading the SGI and SGS, respectively. These corresponded well to the early component of voltage responses that is known to reflect the activation of presynaptic elements, presumably the axonal arborizations and varicosities. Thus, the optically-revealed functional connections between the SGS and SGI were correlated to the morphology.