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Dendritic calcium signaling is central to neural plasticity mechanisms that allow animals to adapt to the environment. Intracellular calcium release (ICR) from the endoplasmic reticulum has long been thought to shape these mechanisms. However, ICR has not been investigated in mammalian neurons in vivo. We combined electroporation of single CA1 pyramidal neurons, simultaneous imaging of dendritic and somatic activity during spatial navigation, optogenetic place field induction, and acute genetic augmentation of ICR cytosolic impact to reveal that ICR supports the establishment of dendritic feature selectivity and shapes integrative properties determining output-level receptive fields. This role for ICR was more prominent in apical than in basal dendrites. Thus, ICR cooperates with circuit-level architecture in vivo to promote the emergence of behaviorally relevant plasticity in a compartment-specific manner.

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Highlights d The axon guidance receptors Robo1/2 can function as synaptogenic cues d Postsynaptic Robo forms a trans-synaptic complex with Slit and presynaptic Neurexin d Robo2 is required for formation of a subset of excitatory CA3 to CA1 synapses d Sparse deletion of Robo2 in CA1 pyramidal neurons impairs emergence of place cells

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