Subset of Thin Spike Cortical Neurons Preserve the Peripheral Encoding of Stimulus Onsets

Abstract

An important question in auditory neuroscience concerns how the neural representation of sound features changes from the periphery to the cortex. Here we focused on the encoding of sound onsets and we used a modeling approach to explore the degree to which auditory cortical neurons follow a similar envelope integration mechanism found at the auditory periphery. Our “forward” model was able to predict relatively accurately the timing of first spikes evoked by natural communication calls in the auditory cortex of awake, head-restrained mice, but only for a subset of cortical neurons. These neurons were systematically different in their encoding of the calls, exhibiting less call selectivity, shorter latency, greater precision, and more transient spiking compared with the same factors of their poorly predicted counterparts. Importantly, neurons that fell into this best-predicted group all had thin spike waveforms, suggestive of suspected interneurons conveying feedforward inhibition. Indeed, our population of call-excited thin spike neurons had significantly higher spontaneous rates and larger frequency tuning bandwidths than those of thick spike neurons. Thus the fidelity of our model's first spike predictions segregated neurons into one earlier responding subset, potentially dominated by suspected interneurons, which preserved a peripheral mechanism for encoding sound onsets and another longer latency subset that reflected higher, likely centrally constructed nonlinearities. These results therefore provide support for the hypothesis that physiologically distinct subclasses of neurons in the auditory cortex may contribute hierarchically to the representation of natural stimuli.