STRFs in primary auditory cortex emerge from masking-based statistics of natural sounds

We investigate how the neural processing in auditory cortex is shaped by the statistics of natural sounds. Hypothesising that auditory cortex (A1) represents the structural primitives out of which sounds are composed, we employ a statistical model to extract such components. The input to the model are cochleagrams which approximate the non-linear transformations a sound undergoes from the outer ear, through the cochlea to the auditory nerve. Cochleagram components do not superimpose linearly, but rather according to a rule which can be approximated using the max function. This is a consequence of the compression inherent in the cochleagram and the sparsity of natural sounds. Furthermore, cochleagrams do not have negative values. Cochleagrams are therefore not matched well by the assumptions of standard linear approaches such as sparse coding or ICA. We therefore consider a new encoding approach for natural sounds, which combines a model of early auditory processing with maximal causes analysis (MCA), a sparse coding model which captures both the non-linear combination rule and non-negativity of the data. An efficient truncated EM algorithm is used to fit the MCA model to cochleagram data. We characterize the generative fields (GFs) inferred by MCA with respect to in vivo neural responses in A1 by applying reverse correlation to estimate spectro-temporal receptive fields (STRFs) implied by the learned GFs. Despite the GFs being non-negative, the STRF estimates are found to contain both positive and negative subfields, where the negative subfields can be attributed to explaining away effects as captured by the applied inference method. A direct comparison with ferret A1 shows many similar forms, and the spectral and temporal modulation tuning of both ferret and model STRFs show similar ranges over the population. In summary, our model represents an alternative to linear approaches for biological auditory encoding while it captures salient data properties and links inhibitory subfields to explaining away effects.Author summary: The information carried by natural sounds enters the cortex of mammals in a specific format: the cochleagram. Instead of representing the original pressure waveforms, the inner ear represents how the energy in a sound is distributed across frequency bands and how the energy distribution evolves over time. The generation of cochleagrams is highly non-linear resulting in the dominance of one sound source per time-frequency bin under natural conditions (masking). Auditory cortex is believed to decompose cochleagrams into structural primitives, i.e., reappearing regular spectro-temporal subpatterns that make up cochleagram patterns (similar to edges in images). However, such a decomposition has so far only been modeled without considering masking and non-negativity. Here we apply a novel non-linear sparse coding model that can capture masking non-linearities and non-negativities. When trained on cochleagrams of natural sounds, the model gives rise to an encoding primarily based-on spectro-temporally localized components. If stimulated by a sound, the encoding units compete to explain its contents. The competition is a direct consequence of the statistical sound model, and it results in neural responses being best described by spectro-temporal receptive fields (STRFs) with positive and negative subfields. The emerging STRFs show a higher similarity to experimentally measured STRFs than a model without masking, which provides evidence for cortical encoding being consistent with the masking based sound statistics of cochleagrams. Furthermore, and more generally, our study suggests for the first time that negative subfields of STRFs may be direct evidence for explaining away effects resulting from performing inference in an underlying statistical model.