Distinct Subthreshold Mechanisms Underlying Rate-Coding Principles in Primate Auditory Cortex

•We developed a novel intracellular recording technique for awake primates•A1 neurons show unique spiking and subthreshold responses to time-varying sounds•Two types of rate-coding A1 neurons exhibited distinct subthreshold responses•Computational model provides mechanistic insights to diverse temporal coding schemes

SummaryA key computational principle for encoding time-varying signals in auditory and somatosensory cortices of monkeys is the opponent model of rate coding by two distinct populations of neurons. However, the subthreshold mechanisms that give rise to this computation have not been revealed. Because the rate-coding neurons are only observed in awake conditions, it is especially challenging to probe their underlying cellular mechanisms. Using a novel intracellular recording technique that we developed in awake marmosets, we found that the two types of rate-coding neurons in auditory cortex exhibited distinct subthreshold responses. While the positive-monotonic neurons (monotonically increasing firing rate with increasing stimulus repetition frequency) displayed sustained depolarization at high repetition frequency, the negative-monotonic neurons (opposite trend) instead exhibited hyperpolarization at high repetition frequency but sustained depolarization at low repetition frequency. The combination of excitatory and inhibitory subthreshold events allows the cortex to represent time-varying signals through these two opponent neuronal populations.