Superoptimal Perceptual Integration Suggests a Place-Based Representation of Pitch at High Frequencies

Pitch, the perceptual correlate of sound repetition rate or frequency, plays an important role in speech perception, music perception, and listening in complex acoustic environments. Despite the perceptual importance of pitch, the neural mechanisms that underlie it remain poorly understood. Although cortical regions responsive to pitch have been identified, little is known about how pitch information is extracted from the inner ear itself. The two primary theories of peripheral pitch coding involve stimulus-driven spike timing, or phase locking, in the auditory nerve (time code), and the spatial distribution of responses along the length of the cochlear partition (place code). To rule out the use of timing information, we tested pitch discrimination of very high-frequency tones (>8 kHz), well beyond the putative limit of phase locking. We found that high-frequency pure-tone discrimination was poor, but when the tones were combined into a harmonic complex, a dramatic improvement in discrimination ability was observed that exceeded performance predicted by the optimal integration of peripheral information from each of the component frequencies. The results are consistent with the existence of pitch-sensitive neurons that rely only on place-based information from multiple harmonically related components. The results also provide evidence against the common assumption that poor high-frequency pure-tone pitch perception is the result of peripheral neural-coding constraints. The finding that place-based spectral coding is sufficient to elicit complex pitch at high frequencies has important implications for the design of future neural prostheses to restore hearing to deaf individuals. SIGNIFICANCE STATEMENT The question of how pitch is represented in the ear has been debated for over a century. Two competing theories involve timing information from neural spikes in the auditory nerve (time code) and the spatial distribution of neural activity along the length of the cochlear partition (place code). By using very high-frequency tones unlikely to be coded via time information, we discovered that information from the individual harmonics is combined so efficiently that performance exceeds theoretical predictions based on the optimal integration of information from each harmonic. The findings have important implications for the design of auditory prostheses because they suggest that enhanced spatial resolution alone may be sufficient to restore pitch via such implants.