Experience-dependent plasticity of excitatory and inhibitory intertectal inputs in Xenopus tadpoles

Abstract

Communication between optic tecta/superior colliculi is thought to be required for sensorimotor behaviors by comparing inputs across the midline; however, the development of and the role of visual experience in the function and plasticity of intertectal connections are unclear. We combined neuronal labeling, in vivo time-lapse imaging, and electrophysiology to characterize the structural and functional development of intertectal axons and synapses in Xenopus tadpole optic tectum. We find that intertectal connections are established early during optic tectal circuit development. We determined the neurotransmitter identity of intertectal neurons using both rabies virus-mediated tracing combined with post hoc immunohistochemistry and electrophysiology. Excitatory and inhibitory intertectal neuronal somata are similarly distributed throughout the tectum. Excitatory and inhibitory intertectal axons are structurally similar and elaborate broadly in the contralateral tectum. We demonstrate that intertectal and retinotectal axons converge onto tectal neurons by recording postsynaptic currents after stimulating intertectal and retinotectal inputs. Cutting the intertectal commissure removes synaptic responses to contralateral tectal stimulation. In vivo time-lapse imaging demonstrated that visual experience drives plasticity in intertectal bouton size and dynamics. Finally, visual experience drives the maturation of excitatory intertectal inputs by increasing AMPA-to- N-methyl-d-aspartate (NMDA) ratios, comparable to experience-dependent maturation of retinotectal inputs, and coordinately increases intertectal GABA receptor-mediated currents. These data indicate that visual experience regulates plasticity of excitatory and inhibitory intertectal inputs, maintaining the balance of excitatory to inhibitory intertectal input. These studies place intertectal inputs as key players in tectal circuit development and suggest that they may play a role in sensory information processing critical to sensorimotor behaviors.