Distributed representation of tone frequency in highly decodable spatio-temporal activity in the auditory cortex

Although the place code of tone frequency, or tonotopic map, has been widely accepted in the auditory cortex, tone-evoked activation becomes less frequency-specific at moderate or high sound pressure levels. This implies that sound frequency is not represented by a simple place code but that the information is distributed spatio-temporally irrespective of the focal activation. In this study, using a decoding-based analysis, we investigated multi-unit activities in the auditory cortices of anesthetized rats to elucidate how a tone frequency is represented in the spatio-temporal neural pattern. We attempted sequential dimensionality reduction (SDR), a specific implementation of recursive feature elimination (RFE) with support vector machine (SVM), to identify the optimal spatio-temporal window patterns for decoding test frequency. SDR selected approximately a quarter of the windows, and SDR-identified window patterns led to significantly better decoding than spatial patterns, in which temporal structures were eliminated, or high-spike-rate patterns, in which windows with high spike rates were selectively extracted. Thus, the test frequency is also encoded in temporal as well as spatial structures of neural activities and low-spike-rate windows. Yet, SDR recruited more high-spike-rate windows than low-spike-rate windows, resulting in a highly dispersive pattern that probably offers an advantage of discrimination ability. Further investigation of SVM weights suggested that low-spike-rate windows play significant roles in fine frequency differentiation. These findings support the hypothesis that the auditory cortex adopts a distributed code in tone frequency representation, in which high- and low-spike-rate activities play mutually complementary roles.