Abstract
The nature of the neural codes for pitch and loudness, two basic auditory attributes, has been a key question in neuroscience for over century. A currently widespread view is that sound intensity (subjectively, loudness) is encoded in spike rates, whereas sound frequency (subjectively, pitch) is encoded in precise spike timing. Here, using information-theoretic analyses, we show that the spike rates of a population of virtual neural units with frequency-tuning and spike-count correlation characteristics similar to those measured in the primary auditory cortex of primates, contain sufficient statistical information to account for the smallest frequency-discrimination thresholds measured in human listeners. The same population, and the same spike-rate code, can also account for the intensity-discrimination thresholds of humans. These results demonstrate the viability of a unified rate-based cortical population code for both sound frequency (pitch) and sound intensity (loudness), and thus suggest a resolution to a long-standing puzzle in auditory neuroscience.
Highlights
The nature of the neural code for perception is a fundamental question in neuroscience [1,2,3,4,5]
A widely held view among auditory scientists is that the neural code for sound intensity involves temporally coarse spike-rate information, whereas the code for sound frequency requires more finegrained and precise spike timing information
Because cortical neurons exhibit relatively broad tuning to frequency and correlated spike counts, it is unclear whether a cortical population code based on spike rates alone can support the remarkably precise pitch-discrimination ability of humans
Summary
The nature of the neural code for perception is a fundamental question in neuroscience [1,2,3,4,5]. The search for the neural code for pitch—an essential perceptual attribute of sound classes such as music and speech—has attracted considerable interest [6,7,8,9]. Timing codes can carry considerably more information than rate codes [12], and the spike times of auditory-nerve fibers have been found to contain more information than needed to account for human listeners’ ability to discriminate very small changes in frequency [11,13,14]. In the primary auditory cortex, single units cannot precisely follow frequencies higher than a few hundred Hertz [15,16,17] – more than an order of magnitude below the upper limit of accurate pitch perception in humans [18,19,20]. Studies in non-human animals found no deficits in pure-tone intensity or frequency discrimination following bilateral ablation of auditory cortex, substantial deficits in pure-tone frequency (pitch) and intensity (loudness) discrimination have been observed in human patients with cortical lesions [21,22], suggesting that the auditory cortex plays an important role in those two perceptual abilities
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