Decoding violated sensory expectations from the auditory cortex of anaesthetized mice: Hierarchical recurrent neural network depicts separate ‘danger’ and ‘safety’ units

Abstract

The ability to respond appropriately to sensory information received from the external environment is among the most fundamental capabilities of central nervous systems. In the auditory domain, processes underlying this behaviour are studied by measuring auditory-evoked electrophysiology during sequences of sounds with predetermined regularities. Identifying neural correlates of ensuing auditory novelty responses is supported by research in experimental animals. In the present study, we reanalysed epidural field potential recordings from the auditory cortex of anaesthetised mice during frequency and intensity oddball stimulation. Multivariate pattern analysis (MVPA) and hierarchical recurrent neural network (RNN) modelling were adopted to explore these data with greater resolution than previously considered using conventional methods. Time-wise and generalised temporal decoding MVPA approaches revealed previously underestimated asymmetry between responses to sound-level transitions in the intensity oddball paradigm, in contrast with tone frequency changes. After training, the cross-validated RNN model architecture with four hidden layers produced output waveforms in response to simulated auditory inputs that were strongly correlated with grand-average auditory-evoked potential waveforms (r2 > 0.9). Units in hidden layers were classified based on their temporal response properties and characterised using principal component analysis and sample entropy. These demonstrated spontaneous alpha rhythms, sound onset and offset responses, and putative 'safety' and 'danger' units activated by relatively inconspicuous and salient changes in auditory inputs, respectively. The hypothesised existence of corresponding biological neural sources is naturally derived from this model. If proven, this would have significant implications for prevailing theories of auditory processing.