Broadband Dynamics Rather than Frequency-Specific Rhythms Underlie Prediction Error in the Primate Auditory Cortex

Abstract

Detection of statistical irregularities, measured as a prediction error response, is fundamental to the perceptual monitoring of the environment. We studied whether prediction error response is associated with neural oscillations or asynchronous broadband activity. Electrocorticography was conducted in three male monkeys, who passively listened to the auditory roving oddball stimuli. Local field potentials (LFPs) recorded over the auditory cortex underwent spectral principal component analysis, which decoupled broadband and rhythmic components of the LFP signal. We found that the broadband component captured the prediction error response, whereas none of the rhythmic components were associated with statistical irregularities of sounds. The broadband component displayed more stochastic, asymmetrical multifractal properties than the rhythmic components, which revealed more self-similar dynamics. We thus conclude that the prediction error response is captured by neuronal populations generating asynchronous broadband activity, defined by irregular dynamic states, which, unlike oscillatory rhythms, appear to enable the neural representation of auditory prediction error response.

Predictive coding of natural images by V1 firing rates and rhythmic synchronization

“…However, our findings appear incompatible with earlier studies that found γ -synchronization to be positively related to prediction errors ( Arnal et al., 2011 ; Bastos et al., 2020 ; Chao et al., 2018 ; Bauer et al., 2014 ). Notably, these studies used temporal predictability, whereas the present study used spatial predictability, and the generalization of our findings to temporal predictability remains to be demonstrated (see Vinck and Bosman, 2016 ; Peter et al., 2019 ; Canales-Johnson et al., 2021 for further discussion). We further note that there are different flavors of predictive coding theories ( Rao and Ballard, 1999 ; Friston, 2008 ; Mumford, 1992 ; Keller and Mrsic-Flogel, 2018 ; de Lange et al., 2018 ; Heeger, 2017 ; Singer, 2021 ).…”

Neural oscillations across olfactory regions encode odorant information in the teleost olfactory system

“…beta and gamma). However, the spectrum of mesoscopic electrophysiological signals (e.g., LFP, EEG) also contains aperiodic or 'arrhythmic' [64][65][66] that have been related to the integration of underlying synaptic currents 67 . Problematically, the standard approach of analyzing periodic power or phase synchronization (e.g., wPLI) through band-pass filtering confounds both periodic and aperiodic activity 68 .…”

The neural dynamics of feedforward and feedback interactions in predictive processing

“…This study did not find evidence for narrow-band gamma oscillations, and found that the increase in LFP gamma power for deviant tones was driven by increases in broad-band power. Additional analyses based on multiscale multifractal analyses suggest that the increase in broad-band energy reflects an underlying aperiodic process (Canales-Johnson et al, 2021a).…”

“…This structure reflects, at least in part, low-pass filtering of synaptic currents in the intracellular space (Pesaran et al, 2018;Einevoll et al, 2013). Rhythms need to be detected against this aperiodic 1/ f a background, which requires the detection of narrow-band peaks (Hermes et al, 2015;Canales-Johnson et al, 2021a;Miller et al, 2009;Donoghue et al, 2020). The observation of synchronized spiking and the identification of a generative circuit is necessary to establish that this peak reflects a locally generated rhythm (Buzsáki et al, 2012;Buzsáki and Schomburg, 2015).…”

“…Auditory stimuli were presented in deviant and standard condition. Deviant auditory stimuli increase event-related-potential (ERP) and broadband LFP power (Canales-Johnson et al, 2021a). Broadband and rhythmic components were identified using principal component analysis.…”