Signature patterns for top-down and bottom-up information processing via cross-frequency coupling in macaque 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 suggests there are differences in message passing up vs. down the cortical hierarchy. These differences result from the linear feedforward of prediction errors, and the nonlinear feedback of predictions. This implies that cross-frequency interactions should predominate top-down. But it remains unknown whether these differences are expressed in cross-frequency interactions in the brain. Here we examined bi-directional 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 (θ, α, β) and low frequency-to-high γ couplings were predominant top-down, while low frequency-to-low γ 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. Our findings suggest the modulatory effect of low frequencies on γ-rhythms in distant regions is important for bi-directional information transfer. The finding of low frequency-to-low γ interactions in the bottom-up direction suggest non-linearities may also play a role in feedforward message passing. Altogether, the patterns of cross-frequency interaction we observed across the auditory hierarchy are largely consistent with the predictive coding framework.

Significance The 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 novel, convenient and computationally advantageous Granger-causal framework to examine bi-directional cross-frequency interactions across four sectors of the auditory cortical hierarchy in macaques. Our findings reveal cross-frequency interactions are predominant in the top-down direction, with important implications for theories of information processing in the brain such as predictive coding. Our findings thereby extend the view of cross-frequency interactions in auditory cortex, suggesting they also play a prominent role in top-down processing.