Outer hair cells (OHCs) provide amplification in the mammalian cochlea using somatic force generation underpinned by voltage-dependent conformational changes of the motor protein prestin. However, prestin must be gated by changes in membrane potential on a cycle-by-cycle basis and the periodic component of the receptor potential may be greatly attenuated by low-pass filtering due to the OHC time constant (τ_m), questioning the functional relevance of this mechanism. Here, we measured τ_m from OHCs with a range of characteristic frequencies (CF) and found that, at physiological endolymphatic calcium concentrations, approximately half of the mechanotransducer (MT) channels are opened at rest, depolarizing the membrane potential to near −40 mV. The depolarized resting potential activates a voltage-dependent K⁺ conductance, thus minimizing τ_m and expanding the membrane filter so there is little receptor potential attenuation at the cell's CF. These data suggest that minimal τ_m filtering in vivo ensures optimal activation of prestin.