Calcium current carried by low voltage-activated, T-type calcium channels is the pacemaker current in a variety of electrically excitable cells. Zona glomerulosa cells (ZG) clustered in rosettes within the outer cortex of the adrenal gland have robust Cav3.2 currents in all recorded species (rat, bovine, mouse, human) including man. We and others have championed the putative role of Cav3.2 window currents (channel activation without full inactivation) to explain how this largely transiently activating calcium channel could provide a tonic current that is sufficient to sustain the production of aldosterone that lasts minutes to hours. Yet, the critical privileged role played by these channels in driving aldosterone production from an electrically quiescent cell that maintains a baseline voltage of ~-85 mV has never been fully reconciled. We now provide new insight into the functional organization of the ZG tissue layer, and the behavior of ZG cells retained within rosettes. We find that in situ ZG cells behave as electrical oscillators and exhibit coordinated activity within the tissue layer. This updated view of calcium signaling in ZG cells provides a satisfying mechanism to explain how Cav3.2 channels generate a significant and recurring calcium signal. It also provides the foundation for recent human genetic studies that have identified somatic gain-of-function mutations in Cav1.3 channels in zona glomerulosa-like aldosterone producing adenomas. Specifically, the large amplitude of voltage oscillations in ZG cells implicates potential roles for high-voltage-activated conductances in the control of aldosterone production, expanding the scope of ionic regulation and the recognition of low renin hypertension as a channelopathy.