It is well known that the medial olivocochlear reflex (MOCR) in the brainstem, part of the efferent network, inhibits the cochlear active gain mechanism. The upstream neural influence of this peripheral inhibition is less understood. When the MOCR is activated, responses generated in the cochlea and cortex undergo putative attenuation, yet the amplitude of responses generated in the brainstem are perplexingly unaffected despite decreased input from the periphery. Based on known neural circuitry, we hypothesized that the inhibition of peripheral input is compensated for by equivalent positive feedback in the brainstem over time. We predicted that the inhibition can be captured at the brainstem with stimuli shorter (1.5 s) than previously employed long durations (4 min) where this inhibition is diminished due to compensation. Results from 18 normal hearing human listeners support our hypothesis in that when the MOCR is activated, there is a robust reduction of responses generated at the periphery, brainstem, and cortex for short stimuli and that brainstem inhibition diminishes for longer stimuli. Our methodology and findings have implications for auditory disorders such as tinnitus, evaluation of efferent function, and provides a novel non-invasive window into potential gain compensation mechanisms in the brainstem.