Two prediction error systems in the nonlemniscal inferior colliculus: 'spectral' and 'non-spectral'

Abstract

According to the predictive processing framework, perception emerges from the reciprocal exchange of predictions and prediction errors (PE) between hierarchically organized neural circuits. The nonlemniscal division of the inferior colliculus (IC) is the earliest source of auditory PE signals, but their neuronal generators, properties and functional relevance have remained mostly undefined. We recorded single-unit mismatch responses to auditory oddball stimulation at different intensities, together with activity evoked by two sequences of alternating tones to control frequency-specific effects. Our results reveal a differential treatment of the unpredictable 'many-standards' control and the predictable 'cascade' control by lemniscal and nonlemniscal IC neurons that is not present in the auditory thalamus or cortex. Furthermore, we found that frequency response areas of nonlemniscal IC neurons reflect their role in subcortical predictive processing, distinguishing 3 hierarchical levels: (1) Nonlemniscal neurons with sharply tuned receptive fields exhibit mild repetition suppression without signaling PEs, thereby constituting the input level of the local predictive processing circuitry. (2) Neurons with broadly tuned receptive fields form the main, 'spectral' PE signaling system, which provides dynamic gain compensation to near-threshold unexpected sounds. This early enhancement of saliency reliant on spectral features was not observed in the auditory thalamus or cortex. (3) Untuned neurons form an accessory, 'non-spectral' PE signaling system, which reports all surprising auditory deviances in a robust and consistent manner, resembling nonlemniscal neurons in the auditory cortex. These nonlemniscal IC neurons show unstructured and unstable receptive fields that could result from inhibitory input controlled by corticofugal projections conveying top-down predictions.Significant Statement Frequency response areas of nonlemniscal neurons in the inferior colliculus correlate with certain predictive processing traits, distinguishing two prediction error systems. The 'spectral' system comprises neurons with broadly tuned receptive fields and is exclusively at play in the nonlemniscal inferior colliculus. It generates prediction errors only to low-intensity deviant sounds and is biased towards ascending changes in frequency. Hence, it provides early gain compensation to near-threshold but informative acoustic events, thereby facilitating efficient auditory discrimination under challenging conditions. The 'non-spectral' PE system reports on unexpected auditory events, uninfluenced by the acoustic spectral characteristics of deviant sounds. This accessory system comprises untuned neurons with disorganized and dynamic receptive fields, which conceivably receive top-down predictions from higher-order levels of the auditory hierarchy.