Stimulus-specific processing of auditory deviants and repetitive stimulus sequences in the human brainstem

Abstract

Auditory deviance detection, the neural process by which unexpected stimuli are identified within repetitive acoustic environments, is crucial for survival. While this phenomenon has been extensively studied in the cortex, recent evidence indicates that it also occurs in subcortical regions, including the inferior colliculus (IC). However, compared to animal studies, research on subcortical deviance detection in humans is often constrained by methodological limitations, leaving several important questions unanswered. This study aims to overcome some of these limitations by employing auditory brainstem responses (ABRs) to investigate the earliest neural correlates of deviance detection in humans, with a focus on the IC. We presented healthy participants of either sex with low- and high-frequency chirps in an oddball paradigm and observed significant deviance detection effects in the ABR, specifically when low-frequency chirps were used as deviants within a context of high-frequency standards. These effects manifested as larger and faster ABRs to deviant stimuli, with the strongest responses occurring at higher stimulation rates. Our findings suggest that the human IC exhibits rapid, stimulus-specific deviance detection with differential modulation of response amplitude and latency. The data indicate that the temporal dynamics of novelty detection in humans align well with the data reported in animals, helping to bridge the gap between animal and human research. By uncovering previously unknown characteristics of subcortical deviance detection in humans, this study highlights the value of ABR recordings with excellent temporal resolution in investigating subcortical deviance detection processes. Significance statementAuditory deviance detection enables the brain to identify unexpected stimuli in a repetitive environment, but its subcortical mechanisms in humans remain comparatively underexplored. Using auditory brainstem responses (ABRs), our study reveals two key findings about deviance detection in the human inferior colliculus (IC). First, we show subcortical deviance detection at latencies under 10 ms, bridging a longstanding gap between human and animal research. Second, deviance detection in the IC is rapid, emerging within three or fewer standard repetitions, with differential modulation of ABR amplitude and latency. These findings improve our understanding of the temporal dynamics of auditory processing in the human IC and highlight the value of ABR recordings in studying subcortical deviance detection mechanisms.