Membrane potential is a ubiquitous cellular feature, underlying important functions including the release of neurotransmitters upon arrival of an action potential, and calcium signaling related to cell proliferation control. Voltage imaging is becoming the standard to investigate membrane potentials, offering significant advantages over electrophysiology: it is less invasive, scalable, and suited to examine intracellular organelles. Although recent imaging implementations capture fast action potentials, they rely on averaging multiple events over a reduced field of view and are limited in temporal resolution. Hence, they can detect the single action potential but miss its propagation dynamics and, significantly, its modulation of synaptic transmission. Furthermore, intracellular propagation of membrane potentials remains unstudied. To overcome these limitations, I propose an all-optical optogenetic approach that leverages “smart” controlling architectures and state-of-the-art detectors to realize a paradigm change: from voltage imaging to on-demand voltage tracking. Upon further developing hardware in the host laboratory, I will investigate the propagation of organellar and plasma membrane potential signals, spontaneous or evoked, in non-excitable cells and neurons. I anticipate that this approach will uncover unprecedented insights into the intra- and inter-cellular signaling mechanisms and their modulation during activity. Indeed, these signatures are hypothesized to be altered by multiple sclerosis and other neurodegenerative diseases, and have so far proved elusive to measure.