The flow of information between cortical regions depends on the excitability at each site, which is reflected in fluctuating field potentials. It remains uncertain how global changes in field potentials affect the latency and strength of cortico-cortical couplings. Therefore, we measured changes in oscillations and inter-regional couplings by recording intracranially from the human cerebral cortex. As participants listened to an auditory narrative, global increases in low-frequency (4-14 Hz) power were associated with stronger and more delayed inter-regional couplings. Conversely, increases in high-frequency power (65+ Hz) were associated with weaker coupling and zero lag. Latency changes were predicted both by local oscillatory power (at each site) and by global oscillatory power (averaged across the cerebral cortex). In network oscillator models, we find these changes in cortico-cortical latency can be generated only at the critical inter-regional coupling strength, showing that there exists a critical balance between the effective influence of inter-regional projections and intra-regional dynamics. Altogether, gradual and widespread increases in low-frequency oscillations were associated with delayed cortico-cortical couplings in the human brain, at the critical inter-regional coupling strength. These changes in inter-regional latency indicate a shift in the timing of peak excitability between regions; we interpret them in relation to bottom-up and top-down information flow, regulated by nonspecific ascending projections to the cortex.