Neural Coding of Periodicity in Marmoset Auditory Cortex

Abstract

Bendor D, Wang X. Neural coding of periodicity in marmoset auditory cortex. J Neurophysiol 103: 1809 -1822, 2010. First published February 10, 2010 doi:10.1152/jn.00281.2009. Pitch, our perception of how high or low a sound is on a musical scale, crucially depends on a sound's periodicity. If an acoustic signal is temporally jittered so that it becomes aperiodic, the pitch will no longer be perceivable even though other acoustical features that normally covary with pitch are unchanged. Previous electrophysiological studies investigating pitch have typically used only periodic acoustic stimuli, and as such these studies cannot distinguish between a neural representation of pitch and an acoustical feature that only correlates with pitch. In this report, we examine in the auditory cortex of awake marmoset monkeys (Callithrix jacchus) the neural coding of a periodicity's repetition rate, an acoustic feature that covaries with pitch. We first examine if individual neurons show similar repetition rate tuning for different periodic acoustic signals. We next measure how sensitive these neural representations are to the temporal regularity of the acoustic signal. We find that neurons throughout auditory cortex covary their firing rate with the repetition rate of an acoustic signal. However, similar repetition rate tuning across acoustic stimuli and sensitivity to temporal regularity were generally only observed in a small group of neurons found near the anterolateral border of primary auditory cortex, the location of a previously identified putative pitch processing center. These results suggest that although the encoding of repetition rate is a general component of auditory cortical processing, the neural correlate of periodicity is confined to a special class of pitch-selective neurons within the putative pitch processing center of auditory cortex.

Neural Mechanisms for the Abstraction and Use of Pitch Information in Auditory Cortex: Figure 1.

“…A cortical region analogous to the pitch region reported by Bendor and Wang (2005) has been identified in several human imaging studies, but has yet to be identified in other animal species for which behavioral evidence of pitch perception is established. But if it does exist, one shall expect to find it in similar low-frequency borders of primary and non-primary cortical fields.…”

“…Approximately 39% of neurons within this anterolateral pitch region were classified as pitch-selective neurons based on multiple criteria. Using temporally jittered click trains and iterated rippled noises, Bendor and Wang (2010) further demonstrated that these pitch-selective neurons were sensitive to the temporal regularity of sounds, unlike modulation-sensitive neurons outside the pitch area, which are instead tuned to repetition rate regardless of the waveform's temporal regularity. A recent study has reported evidence of pitch perception by marmosets (Osmanski et al, 2011).…”

“…Cortical areas with an orderly tonotopic organization, like A1, can represent pitch in frequency regions corresponding to individual harmonic components, orthogonal to the tonotopic axis (Langer et al, 1997). Alternatively, pitch can be extracted by neurons tuned to low frequencies in a tonotopically organized cortical area (Bendor and Wang, 2005) or in a specialized cortical region (Griffiths and Hall, 2012). One would also like to know in any of such scenarios whether a representation of pitch can be generalized to all types of sounds bearing the same pitch (including missing fundamental sounds), and whether a particular neural representation is linked to pitch perception measured behaviorally.…”

“…For a subset of these neurons, feature representations were multiplexed within separate response time windows, so the pitch and timbre of vowels can be invariantly represented in a single auditory cortical neuron (Walker et al, 2011). It may therefore be instructive for future studies to examine pitch tuning in multiple time windows throughout a neuron's response to sounds, since tuning properties across the onset, sustained, and offset windows can be fundamentally different (Wang et al 2005).…”

“…Such neurons may be distributed throughout the auditory cortex, but human imaging studies suggest that pitch neurons are likely to be concentrated in a region of auditory cortex that is specialized to encode the periodicity of temporally regular sounds (Griffiths and Hall, 2012). Bendor and Wang (2005) have provided evidence for pitch extraction by single neurons in the auditory cortex of awake marmosets. "Pitch-selective neurons" described in this study were defined as those whose CF for pure tones matched their periodicity tuning for missing fundamental harmonic complex sounds, where the spectral components of the latter all lay outside of the neuron's excitatory-frequency response area.…”