The neuronal representation of pitch in primate auditory cortex

Daniel Bendor and Xiaoqin Wang

Nature, 2005 Aug 25, 436 (7054), 1161-1165

Laboratory of Auditory Neurophysiology, Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, Maryland 21025, USA.

Abstract:

Pitch perception is critical for identifying and segregating auditory objects, especially in the context of music and speech. The perception of pitch is not unique to humans and has been experimentally demonstrated in several animal species. Pitch is the subjective attribute of a sound's fundamental frequency (f(0)) that is determined by both the temporal regularity and average repetition rate of its acoustic waveform. Spectrally dissimilar sounds can have the same pitch if they share a common f(0). Even when the acoustic energy at f(0) is removed ('missing fundamental') the same pitch is still perceived. Despite its importance for hearing, how pitch is represented in the cerebral cortex is unknown. Here we show the existence of neurons in the auditory cortex of marmoset monkeys that respond to both pure tones and missing fundamental harmonic complex sounds with the same f(0), providing a neural correlate for pitch constancy. These pitch-selective neurons are located in a restricted low-frequency cortical region near the anterolateral border of the primary auditory cortex, and is consistent with the location of a pitch-selective area identified in recent imaging studies in humans. (Bold text emphasis by Martin Braun)

Comment:

Pitch neurons had previously been recorded in the auditory midbrain, i.e. two synaptic levels below the primary auditory cortex, by Biebel and Langner (1997 and 2002). The new findings of Bendor and Wang agree well with the earlier ones, and they provide an important missing link for the hypothesis of Langner (1992) that pitch is extracted by periodicity analysis in the midbrain and then coded, and transmitted up to the cortex, as part of the low-frequency section of the auditory neural pathway. While the exact location of the now discovered pitch neurons in the cortex remains to be determined by future anatomical studies, the new physiological data indicate that they may not only be present in the low-frequency section of the primary auditory cortex, but also in adjacent low-frequency sections of secondary auditory fields. Such a distribution would agree with the important role of pitch in the high-order processes that underlie sound identification and acoustic communication.

An interesting detail of the new results is the following one: When partials 6 and 7 of the complex tone stimulus were the two lowest ones, pitch salience, as measured in neuronal firing rate, was still optimum. But when partials 7 and 8 were the two lowest ones, pitch salience was clearly sub-optimum (Fig. 4c). This breakpoint in pitch salience above partial 7 agrees exactly with psychoacoustic data from humans for the pitch range of the central octave of music (C4-C5). This finding adds to previous data suggesting that the origin of the breakpoint lies in the laminar architecture of the auditory midbrain (Braun, 1999). Because the cochlea is smaller in marmosets than in humans, frequency resolution at this level is likely to be better in humans. But frequency resolution at the midbrain level, which apparently determines the contribution of partials in pitch detection (Braun, 1999), may be very similar in both species. (Comment Martin Braun)

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