Comprehensive imaging of synaptic activity reveals dendritic growth rules that cluster inputs

The distribution of synapses across dendritic arbors determines their contribution to neural computations since nonlinear conductances amplify co-active clustered inputs. To determine whether, and how patterned synaptic topography arises during development we developed a random-access microscope capable of full-neuron calcium imaging of activity and structural plasticity of developing neurons in awake Xenopus tadpoles. By imaging growing brain neurons in response to plasticity-inducing visual training, we show coordinated growth and synaptogenesis specific to each neurons spike tuning. High evoked activity in neurons tuned to the trained stimulus induced pruning of non-driven inputs across the dendritic arbor as these neurons strengthened their responses to this stimulus. In stark contrast, initially unresponsive neurons that shifted their spike tuning toward the trained stimulus exhibited localized growth and new responsive synapses near existing active inputs. These information-driven growth rules promote clustering of synapses tuned to a developing neurons emerging receptive field. One-Sentence SummarySensory input directs brain neuronal growth and connectivity promoting clustering of synaptic inputs tuned to a neurons encoding properties.