The cochlea's capacity to decode sound frequencies is enhanced by a unique structural arrangement along its longitudinal axis, a feature termed 'tonotopy' or place coding. Auditory hair cells at the cochlea's base are activated by high-frequency sounds, while those at the apex respond to lower frequencies. Presently, our understanding of tonotopy primarily hinges on electrophysiological, mechanical, and anatomical studies conducted in animals or human cadavers. However, direct in vivo measurements of tonotopy in humans have been elusive due to the invasive nature of these procedures. This absence of live human data has posed an obstacle in establishing an accurate tonotopic map for patients, potentially limiting advancements in cochlear implant and hearing enhancement technologies. In this study, we conducted acoustically-evoked intracochlear recordings in 50 human subjects using a longitudinal multi-electrode array. These electrophysiological measures, combined with postoperative imaging to accurately locate the electrode contacts allow us to create the first in vivo tonotopic map of the human cochlea. Furthermore, we examined the influences of sound intensity, electrode array presence, and the creation of an artificial third window on the tonotopic map. Our findings reveal a significant disparity between the tonotopic map at daily speech conversational levels and the conventional (i.e., Greenwood) map derived at close-to-threshold levels. Our findings have implications for advancing cochlear implant and hearing augmentation technologies, but also offer novel insights into future investigations into auditory disorders, speech processing, language development, age-related hearing loss, and could potentially inform more effective educational and communication strategies for those with hearing impairments.
Significance statement: The ability to discriminate sound frequencies, or pitch, is vital for communication and facilitated by a unique arrangement of cells along the cochlear spiral (tonotopic place). While earlier studies have provided insight into frequency selectivity based on animal and human cadaver studies, our understanding of the in vivo human cochlea remains limited. Our research offers, for the first time, in vivo electrophysiological evidence from humans, detailing the tonotopic organization of the human cochlea. We demonstrate that the functional arrangement in humans significantly deviates from the conventional Greenwood function, with the operating point of the in vivo tonotopic map showing a basal (or frequency downward) shift. This pivotal finding could have far-reaching implications for the study and treatment of auditory disorders.