Spontaneous activity in the brain maintains an internal structured pattern that reflects the external environment, which is essential for processing information and developing perception and cognition. An essential prerequisite of spontaneous activity for perception is the ability to reverberate external information, such as by potentiation. Yet its role in the processing of potentiation in mouse superior colliculus (SC) neurons is less studied. Here, we used electrophysiological recording, optogenetics, and drug infusion methods to investigate the mechanism of potentiation in SC neurons. We found that visual experience potentiated SC neurons several minutes later in different developmental stages, and the similarity between spontaneous and visually-evoked activity increased with age. Before eye-opening, activation of retinal ganglion cells that expressed ChR2 also induced the potentiation of spontaneous activity in the mouse SC. Potentiation was dependent on stimulus number and showed feature selectivity for direction and orientation. Optogenetic activation of parvalbumin neurons in the SC attenuated the potentiation induced by visual experience. Furthermore, potentiation in SC neurons was blocked by inhibiting the glutamate transporter GLT1. These results indicated that the potentiation induced by a visual stimulus might play a key role in shaping the internal representation of the environment, and serves as a carrier for short-term memory consolidation.
Keywords: Feature selectivity; Glutamate homeostasis; Potentiation; Spontaneous activity; Superior colliculus; Visual experience.