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Neural activity plays an important role in development and maturation of visual circuits in the brain. Activity can be instructive in refining visual projections by directly mediating formation and elimination of specific synaptic contacts through competition-based mechanisms. Alternatively, activity could be permissive-regulating production of factors that create a favorable environment for circuit refinement. Here we used the Xenopus laevis tadpole visual system to test whether activity is instructive or permissive for shaping development of the retinotectal circuit. In vivo spike output was dampened in a small subgroup of tectal neurons, starting from developmental stages 44-46, by overexpressing Shaker-like Xenopus Kv1.1 potassium channels using electroporation. Tadpoles were then reared until stage 49, a time period when significant refinement of the retinotectal map occurs. Kv1.1-expressing neurons had significantly decreased spike output in response to both current injection and visual stimuli compared to untransfected controls, with spiking occurring during a more limited time interval. We found that Kv1.1-expressing neurons had larger visual receptive fields, decreased receptive field sharpness, and more persistent recurrent excitation than control neurons, all of which are characteristics of immature neurons. Transfected cells, however, had normal spontaneous excitatory synaptic currents and dendritic arbors. These results suggest that spike output of a tectal neuron plays an important instructive role in development of its receptive field properties and refinement of local circuits. However, other activity-dependent processes, such as synaptogenesis and dendritic growth, remain unaffected due to the permissive environment created by otherwise normal network activity.
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