Enhanced Visual Activity In Vivo Forms Nascent Synapses in the Developing Retinotectal Projection

Abstract

Patterned neural activity during development is critical for proper wiring of sensory circuits. Previous work demonstrated that exposing freely swimming Xenopus tadpoles to 4 h of enhanced visual stimulation accelerates the dendritic growth rate of optic tectal neurons in vivo. Here we test whether this same period of visual stimulation increased synaptic maturation and formation of new synapses in the retinotectal pathway. We assessed synaptic properties of stage 48 tadpoles that were exposed to a simulated-motion stimulus for 4–5 h. Based on our findings that immature retinotectal synapses have greater paired-pulse facilitation compared with more mature synapses, consistent with a lower release probability (Pr), we used a paired-pulse protocol to elicit responses selectively from nascent synapses with low Pr. Although AMPA/NMDA ratios for single and paired stimuli were the same in control tadpoles, visual stimulation caused a relative decrease in the AMPA/NMDA ratio of the paired response. We evoked retinotectal synaptic transmission in the presence of Sr2+to record asynchronous vesicle release. We compared evoked mEPSCs induced by single and paired stimuli and found that visual stimulation selectively enhances the amplitude and number of AMPA receptor (AMPAR)–mediated mEPSCs evoked by paired stimuli relative to those evoked by single stimuli. Together these results show that enhanced visual stimulation affects both AMPAR- and NMDAR-mediated responses in a population of synapses revealed by paired-pulse stimulation. This suggests that in vivo visual stimulation increases synapses that have a low Pr and that have properties consistent with immature synapses.