Neural representation of harmonic complex tones in primary auditory cortex of the awake monkey

Many natural sounds are periodic and consist of frequencies (harmonics) that are integer multiples of a common fundamental frequency (F0). Such harmonic complex tones (HCTs) evoke a pitch corresponding to their F0, which plays a key role in the perception of speech and music. "Pitch-selective" neurons have been identified in non-primary auditory cortex of marmoset monkeys. Noninvasive studies point to a putative "pitch center" located in a homologous cortical region in humans. It remains unclear whether there is sufficient spectral and temporal information available at the level of primary auditory cortex (A1) to enable reliable pitch extraction in non-primary auditory cortex. Here we evaluated multiunit responses to HCTs in A1 of awake macaques using a stimulus design employed in auditory nerve studies of pitch encoding. The F0 of the HCTs was varied in small increments, such that harmonics of the HCTs fell either on the peak or on the sides of the neuronal pure tone tuning functions. Resultant response-amplitude-versus-harmonic-number functions ("rate-place profiles") displayed a periodic pattern reflecting the neuronal representation of individual HCT harmonics. Consistent with psychoacoustic findings in humans, lower harmonics were better resolved in rate-place profiles than higher harmonics. Lower F0s were also temporally represented by neuronal phase-locking to the periodic waveform of the HCTs. Findings indicate that population responses in A1 contain sufficient spectral and temporal information for extracting the pitch of HCTs by neurons in downstream cortical areas that receive their input from A1.