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

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.

Evidence for plasticity of intertectal neuronal connections in adult Xenopus

Each optic tectum in Xenopus receives two visuotectal projections of the binocular portion of the visual world, one from each eye. These two visuotectal projections at each optic tectum are superimposed and in register, an arrangement made possible by the functional organization of a topographically ordered system of intertectal neuronal connections. Following surgical rotation of a larval eye in Xenopus a rearrangement of intertectal connections may take place during metamorphosis. The nature of the intertectal reorganization is such that the two visuotectal projections at each optic tectum remain in register. This synaptic reorganization requires visual experience. The capacity of the intertectal system to respond to such changes in interocular geometry reduces with age but even in adult life a residual plasticity of intertectal connections exists. In the adult animal an acute rotation of one eye by 90° evokes no reorganization of intertectal connections. An equivalent cumulative change in interocular relationship in adult life which is achieved very gradually rather than acutely can, however, lead to an appropriate reorganization of intertectal connections. It is suggested that the normal role of this residual intertectal plasticity is to compensate for the normal changes in interocular geometry that occur with growth in the post-metamorphic animal.

The time course of experience-dependent synaptic switching of visual connections in Xenopus laevis

Following the rotation of one larval eye in Xenopus laevis , the pattern of functional connections linking the two optic tecta may change. The time necessary for the elaboration of the new pattern of connections was studied by mapping the connections at various time intervals after the right eye had been rotated by 90°, this eye rotation being performed at stage 63. The minimal time necessary for the emergence of a new pattern of intertectal connections was of the order of 8-12 days. Visual deprivation during this period prevented the development of a new pattern of intertectal connections.