A two-level hierarchy underlies auditory novelty processing in the human brain

Predictive coding theory proposes a hierarchical framework for auditory novelty processing, with multiple brain regions involved. However, how these regions are organized spatiotemporally within the auditory hierarchy remains unclear. To address this issue, we deployed a passive pure tone oddball paradigm in a group of patients with stereoelectroencephalography recording for epilepsy treatment. Event-related high frequency activity was elicited by novel auditory stimuli across multiple brain regions. Based on latency, these regions could be segregated into a two-level hierarchy, with the temporal, insular, and parietal regions at the lower level and the frontal and hippocampal regions at the higher level. The lower, but not the higher, level showed a significant response to standard stimuli. Granger causality analysis further indicated that bidirectional connectivity between levels was asymmetrically modulated. The bottom-up connections were constant, whereas top-down connections were selectively modulated by novel stimuli. These results are consistent with a mechanism in which the lower level transmits auditory signals to the higher level, where comparison is made and potential prediction updating is triggered upon novelty detection. Such prediction updating would be mediated by dynamically modulated top-down pathways. Together, our findings are compatible with a two-level spatiotemporal hierarchical model for auditory novelty processing.