Sound-evoked compound action potential (CAP), which captures the synchronous activation of the auditory nerve fibres (ANFs), is commonly used to probe deafness in experimental and clinical settings. All ANFs are believed to contribute to CAP threshold and amplitude: low sound-pressure levels activate the high-spontaneous rate (SR) fibres, and increasing levels gradually recruit medium- and then low-SR fibres. Here, we quantitatively analyze the contribution of the ANFs to CAP 6 days after 30 min-infusion of ouabain into the round window niche. Anatomical examination showed a progressive ablation of ANFs, following increasing concentration of ouabain. CAP amplitude and threshold plotted against ANFs loss revealed 3 ANF pools: i) a highly ouabain-sensitive pool, which does not participate either in the CAP threshold or in the amplitude, ii) a less sensitive pool, which only encoded CAP amplitude, and iii) a resistant pool to ouabain, required for CAP threshold and amplitude. Remarkably, the 3 pools distribution was similar to the SR-based ANF distribution (low-, medium- and high-SR fibers), suggesting that the low-SR fibres loss leaves the CAP unaffected. Single-unit recordings from the auditory nerve confirmed this hypothesis, and further showed that it is due to their delayed and broad first spike latency distribution. In addition to unraveling the neural mechanisms that encode CAP, our computational simulation of an assembly of guinea pig ANFs, generalizes and extends our experimental findings to different species of mammals. Altogether our data demonstrated that substantial auditory nerve fibre loss can co-exist with normal hearing threshold, and even unchanged CAP amplitude.