The Role of Inhibition in a Computational Model of an Auditory Cortical Neuron during the Encoding of Temporal Information

In auditory cortex, temporal information within a sound is represented by two complementary neural codes: a temporal representation based on stimulus-locked firing and a rate representation, where discharge rate co-varies with the timing between acoustic events but lacks a stimulus-synchronized response. Using a computational neuronal model, we find that stimulus-locked responses are generated when sound-evoked excitation is combined with strong, delayed inhibition. In contrast to this, a non-synchronized rate representation is generated when the net excitation evoked by the sound is weak, which occurs when excitation is coincident and balanced with inhibition. Using single-unit recordings from awake marmosets (Callithrix jacchus), we validate several model predictions, including differences in the temporal fidelity, discharge rates and temporal dynamics of stimulus-evoked responses between neurons with rate and temporal representations. Together these data suggest that feedforward inhibition provides a parsimonious explanation of the neural coding dichotomy observed in auditory cortex.Author Summary: How does our auditory system represent time within a sound? Previous work has demonstrated that both the firing rate of neurons (rate code) and the timing of their stimulus-evoked responses (temporal code) can be used by auditory cortical neurons to represent temporal information. We investigated the underlying mechanisms of these two neural representations using a computational model of a cortical neuron. We found that the timing and magnitude of inhibition determined whether neurons responded to an acoustic stimulus using a rate or temporal code. Our model predicts several differences in the response pattern of neurons using rate and temporal representations, which we next validated with electrophysiological data recorded from the auditory cortex of non-human primates. Together these data suggest that feedforward inhibition provides a parsimonious explanation of how rate and temporal representations are generated in auditory cortex.