Cortical mapping of mismatch responses to independent acoustic features

Predictive coding is an influential theory of neural processing underlying perceptual inference. However, it is unknown to what extent prediction violations of different sensory features are mediated in different regions in auditory cortex, with different dynamics, and by different mechanisms. This study investigates the neural responses to synthesized acoustic syllables, which could be expected or unexpected, along several features. By using electrocorticography (ECoG) in rat auditory cortex (subjects: adult female Wistar rats with normal hearing), we aimed at mapping regional differences in mismatch responses to different stimulus features. Continuous streams of morphed syllables formed roving oddball sequences in which each stimulus was repeated several times (thereby forming a standard) and subsequently replaced with a deviant stimulus which differed from the standard along one of several acoustic features: duration, pitch, interaural level differences (ILD), or consonant identity. Each of these features could assume one of several different levels, and the resulting change from standard to deviant could be larger or smaller. The deviant stimuli were then repeated to form new standards. We analyzed responses to the first repetition of a new stimulus (deviant) and its last repetition in a stimulus train (standard). For the ECoG recording, we implanted urethane-anaesthetized rats with 8 × 8 surface electrode arrays covering a 3 × 3 mm cortical patch encompassing primary and higher-order auditory cortex. We identified the response topographies and latencies of population activity evoked by acoustic stimuli in the rat auditory regions, and mapped their sensitivity to expectation violations along different acoustic features. For all features, the responses to deviant stimuli increased in amplitude relative to responses to standard stimuli. Deviance magnitude did not further modulate these mismatch responses. Mismatch responses to different feature violations showed a heterogeneous distribution across cortical areas, with no evidence for systematic topographic gradients for any of the tested features. However, within rats, the spatial distribution of mismatch responses varied more between features than the spatial distribution of tone-evoked responses. This result supports the notion that prediction error signaling along different stimulus features is subserved by different cortical populations, albeit with substantial heterogeneity across individuals.