Understanding the information processing performed by a single neuron requires the monitoring of physiological dynamics from a variety of subcellular compartments including dendrites and axons. In this study, we showed that the expression of a fusion protein, consisting of a Ca²⁺ indicator protein (G-CaMP6) and a cytoskeleton protein (actin), enabled large-scale recording of Ca²⁺ dynamics from hundreds of postsynaptic spines and presynaptic boutons in a cortical pyramidal cell. At dendritic spines, G-CaMP6-actin had the potential to detect localized Ca²⁺ activity triggered by subthreshold synaptic inputs. Back-propagating action potentials reliably induced Ca²⁺ fluorescent increases in all spines. At axonal boutons, G-CaMP6-actin reported action potential trains propagating along axonal collaterals. The detectability of G-CaMP6-actin should contribute toward a deeper understanding of neural network architecture and dynamics at the level of individual synapses.