Functional Clustering Drives Encoding Improvement in a Developing Brain Network during Awake Visual Learning

Abstract

Sensory experience drives dramatic structural and functional plasticity in developing neurons. However, for single-neuron plasticity to optimally improve whole-network encoding of sensory information, changes must be coordinated between neurons to ensure a full range of stimuli is efficiently represented. Using two-photon calcium imaging to monitor evoked activity in over 100 neurons simultaneously, we investigate network-level changes in the developing Xenopus laevis tectum during visual training with motion stimuli. Training causes stimulus-specific changes in neuronal responses and interactions, resulting in improved population encoding. This plasticity is spatially structured, increasing tuning curve similarity and interactions among nearby neurons, and decreasing interactions among distant neurons. Training does not improve encoding by single clusters of similarly responding neurons, but improves encoding across clusters, indicating coordinated plasticity across the network. NMDA receptor blockade prevents coordinated plasticity, reduces clustering, and abolishes whole-network encoding improvement. We conclude that NMDA receptors support experience-dependent network self-organization, allowing efficient population coding of a diverse range of stimuli. In the developing brain, sensory experience can extensively re-wire neurons, determining both their shape and function. It is thought that this early period of plasticity improves the brain's representation of sensory input. For this plasticity to actually improve coding efficiency, changes to individual neurons should be coordinated across the brain to produce a network-level functional organization. In this study, we measure such network-level changes during visual learning in developing Xenopus laevis (frog) tadpoles. By imaging neuronal calcium levels, we track activity in over 100 neurons simultaneously to observe changes in both single neurons and whole networks during training. We find that the network improves its representation of visual stimuli over time, by forming spatial clusters of highly connected, similarly responding neurons. Distant neurons, however, become less connected. This organization improves the ability of large groups of neurons, spanning multiple clusters, to discriminate the trained stimuli. Finally, we show that blockade of the NMDA receptor prevents this functional organization and the improvement in the network's stimulus representation. Our study shows how developmental plasticity can influence not only the proper connectivity of the visual system, but also its coding capacity.