An ultimate goal of neuroscience is to understand how the nervous system encodes and processes information about environment and experience, and how neuronal activity leads to perception and behavior. Recent advances in optical approaches including optogenetics and in vivo calcium imaging allow neuroscientists to manipulate and observe neuronal circuits in detail, shedding light into this central question. Hybrid voltage sensor (hVOS), a genetically-encoded voltage indicator (GEVI), offers direct readout of membrane potentials from single cells and subcellular compartments with sub-millisecond temporal resolution, providing unique insights into neural circuits that are challenging to study via calcium imaging or electrophysiology. In my dissertation I employed hVOS imaging to unravel dentate gyrus and cochlear nuclei circuitry. We took advantage of an axonal-targeting hVOS probe to evaluate action potential (AP) dynamics in fine axons inaccessible to patch-clamping. We identified activity-dependent AP broadening in dentate granule cell (GC) axons and also for the first time in mossy cell (MC) axons, which may contribute to short term plasticity of neural circuits. Next, we used Cre-lox technology to label genetically-defined neurons with the hVOS probe. We were able to demonstrate how subpopulations of dentate GCs responded to a novel environment, and how voluntary running affected presynaptic inputs to adult-born GCs. With the same strategy we investigated MC wiring in hippocampus and provided experimental evidence that MCs may excite other MCs, a microcircuit which may be critical for dentate gyrus function. We also showed potentiation between neurons within an iso-frequency lamina in the posteroventral cochlear nucleus. In summary, this dissertation has revealed information processing in neuronal microcircuits and subcellular compartments in hippocampus and cochlear nuclei with a novel imaging method. hVOS as a GEVI enables neuroscientists to further explore how the nervous system operates at different levels from axons and dendrites to intact brain tissue.