Flexible control of motor timing is crucial for behavior. Before volitional movement begins, frontal cortex and striatum exhibit ramping spiking activity, with variable ramp slopes anticipating movement onsets. This activity in the cortico-basal ganglia loop may function as an adjustable ‘timer’, triggering actions at the desired timing. However, because the frontal cortex and striatum share similar ramping dynamics and are both necessary for timing behaviors, distinguishing their individual roles in this timer function remains challenging. To address this fundamental gap, we introduced two-region dynamical system models to design experiments distinguishing the roles of each brain area. Specifically, these models generate ramping dynamics via temporal integration through positive feedback connections. Guided by these models, we conducted transient perturbation experiments with large-scale electrophysiology (7070 neurons, 59 mice) in mice performing a flexible lick timing task. Following transient silencing of the frontal cortex, cortical and striatal activity swiftly returned to pre-silencing levels and resumed ramping, leading to a shift in lick timing close to the silencing duration. Conversely, briefly inhibiting the striatum caused a gradual decrease in ramping activity in both regions, with ramping resuming from reduced levels post-inhibition, shifting lick timing beyond the inhibition duration. Thus, inhibiting the frontal cortex and striatum paused and rewound the timer, respectively, distinguishing their roles in motor timing. These findings are consistent with models where the striatum is part of an integrator, generating ramping activity representing time, while the frontal cortex provides inputs to the striatal integrator to adjust action timing. Notably, transient perturbations of the frontal cortex and striatum had graded and lasting impacts on ramping activity and lick timing, providing causal evidence for integrator dynamics in generating ramping activity. Altogether, we identified the mechanism of the ‘timer’ in the brain at both algorithmic (integrator dynamics) and implementation levels (different roles of cortex vs. striatum).