Correct tonotopic representation is necessary for complex pitch perception

Abstract

The ability to extract a pitch from complex harmonic sounds, such as human speech, animal vocalizations, and musical instruments, is a fundamental attribute of hearing. Some theories of pitch rely on the frequency-to-place mapping, or tonotopy, in the inner ear (cochlea), but most current models are based solely on the relative timing of spikes in the auditory nerve. So far, it has proved to be difficult to distinguish between these two possible representations, primarily because temporal and place information usually covary in the cochlea. In this study, ''transposed stimuli'' were used to dissociate temporal from place information. By presenting the temporal information of low-frequency sinusoids to locations in the cochlea tuned to high frequencies, we found that human subjects displayed poor pitch perception for single tones. More importantly, none of the subjects was able to extract the fundamental frequency from multiple low-frequency harmonics presented to high-frequency regions of the cochlea. The experiments demonstrate that tonotopic representation is crucial to complex pitch perception and provide a new tool in the search for the neural basis of pitch. P itch is one of the primary attributes of auditory sensation, playing a crucial role in music and speech perception, and in analyzing complex auditory scenes (1, 2). For most sounds, pitch is an emergent perceptual property, formed by the integration of many harmonically related components into a single pitch, usually corresponding to the sound's fundamental frequency (F0). The ability to extract the F0 from a complex tone, even in the absence of energy at the F0 itself, is shared by a wide variety of species (3, 4) and is present from an early developmental stage in humans (5).The question of how pitch is encoded by the auditory system has a long and distinguished history, with lively debates on the subject going back to the time of Ohm (6) and Helmholtz (7). Although the debate has evolved considerably since its inception, one of the basic questions, whether timing (8, 9) or place information (10-12) (or both) from the cochlea is used to derive pitch, remains basically unanswered. In recent years, the weight of opinion and investigation has favored temporal codes (13-17). With few exceptions (18), recent models of pitch perception have been based solely on the timing information available in the interspike intervals represented in the simulated (17,(19)(20)(21) or actual (22, 23) auditory nerve. Such temporal models derive a pitch estimate by pooling timing information across auditorynerve fibers without regard to the frequency-to-place mapping (tonotopic organization) of the peripheral auditory system.Temporal models of pitch perception are attractive for at least two reasons. First, they provide a unified and parsimonious way of dealing with a diverse range of pitch phenomena (20). Second, the postulated neural mechanisms are essentially identical to those required of the binaural system when performing interaural timing comparisons for spatial loc...

Topographic organization is essential for pitch perception

“…When the ear receives this modulated high-frequency carrier, it directs it to the 4-kHz place, where it becomes subsequently demodulated at the cochlea͞nerve interface, resulting in low-frequency modulated responses on the nerve. Bernstein (6) and Oxenham et al (1) confirm this scenario and the integrity of the lowfrequency modulations by demonstrating that they in fact are induced at their new places with sufficient fidelity to serve accurate binaural localization (Experiment 1).…”

“…Oxenham et al (1) then proceed to the heart of this study to demonstrate that transposing temporally modulated waveforms to arbitrary tonotopic locations has a severe impact on the perceived pitch. Subjects were largely unable to compare the pitch of the transposed stimuli to those of regular harmonics (Experiment 2), nor were they able to assign them a clear pitch value by matching it to the frequency of a pure tone (Experiment 3).…”

“…This uncertainty has generated passionate debates between the proponents of two very different theories of pitch, one based on the place or location of neural activation patterns, and the other on their temporal modulations. This state of affairs is now likely to change dramatically in favor of the place theories with the publication of results of intricately designed psychoacoustic experiments by Oxenham et al (1) reported in this issue of PNAS.…”

“…Against the backdrop of this controversy come the ingenious experiments by Oxenham et al (1) to offer a simple unambiguous test of the two theories. …”

Cochlear implants: A remarkable past and a brilliant future

“…Among the features, the presentation and perception of the resolved harmonics appears to be essential for highly-salient pitch percepts in normal hearing (Oxenham et al, 2004). In addition, the harmonics may need to be at the "tonotopically correct" places along the cochlear partition to be effective.…”