Distinct cross-frequency coupling signatures for top-down and bottom-up information processing in auditory cortex

Abstract

Predictive coding is a theoretical framework that provides a functional interpretation of top-down and bottom up interactions in sensory processing. The theory has suggested that specific frequency bands relay bottom-up and top-down information (e.g. \"{gamma} up, {beta} down\"). But it remains unclear whether this notion generalizes to cross-frequency interactions. Furthermore, most of the evidence so far comes from visual pathways. Here we examined cross-frequency coupling across four sectors of the auditory hierarchy in the macaque. We computed two measures of cross-frequency coupling, phase-amplitude coupling (PAC) and amplitude-amplitude coupling (AAC). Our findings revealed distinct patterns for bottom-up and top-down information processing among cross-frequency interactions. Both top-down and bottom-up made prominent use of low frequencies: low-to-low frequency ({theta}, , {beta}) and low frequency-to-high {gamma} couplings were predominant top-down, while low frequency-to-low {gamma} couplings were predominant bottom-up. These patterns were largely preserved across coupling types (PAC and AAC) and across stimulus types (natural and synthetic auditory stimuli), suggesting they are a general feature of information processing in auditory cortex. Moreover, our findings showed that low-frequency PAC alternated between predominantly top-down or bottom-up over time. Altogether, this suggests sensory information need not be propagated along separate frequencies upwards and downwards. Rather, information can be unmixed by having low frequencies couple to distinct frequency ranges in the target region, and by alternating top-down and bottom-up processing over time.\n\n1 SignificanceThe brain consists of highly interconnected cortical areas, yet the patterns in directional cortical communication are not fully understood, in particular with regards to interactions between different signal components across frequencies. We employed a a unified, computationally advantageous Granger-causal framework to examine bi-directional cross-frequency interactions across four sectors of the auditory cortical hierarchy in macaques. Our findings extend the view of cross-frequency interactions in auditory cortex, suggesting they also play a prominent role in top-down processing. Our findings also suggest information need not be propagated along separate channels up and down the cortical hierarchy, with important implications for theories of information processing in the brain such as predictive coding.