Abstract

The arrival of sound signals in the auditory cortex (AC) triggers both local and inter-regional signal propagations over time up to hundreds of milliseconds and builds up both intrinsic functional connectivity (iFC) and extrinsic functional connectivity (eFC) of the AC. However, interactions between iFC and eFC are largely unknown. Using intracranial stereo-electroencephalographic recordings in people with drug-refractory epilepsy, this study mainly investigated the temporal dynamic of the relationships between iFC and eFC of the AC. The results showed that a Gaussian wideband-noise burst markedly elicited potentials in both the AC and numerous higher-order cortical regions outside the AC (non-auditory cortices). Granger causality analyses revealed that in the earlier time window, iFC of the AC was positively correlated with both eFC from the AC to the inferior temporal gyrus and that to the inferior parietal lobule. While in later periods, the iFC of the AC was positively correlated with eFC from the precentral gyrus to the AC and that from the insula to the AC. In conclusion, dual-directional interactions occur between iFC and eFC of the AC at different time windows following the sound stimulation and may form the foundation underlying various central auditory processes, including auditory sensory memory, object formation, integrations between sensory, perceptional, attentional, motor, emotional, and executive processes.

Highlights

  • In humans, passive listening to sound stimuli activates both the auditory cortex (AC) and some cortical regions that do not belong to the typical auditory system (Ackermann et al, 2001; Brown et al, 2004; Londei et al, 2007)

  • In this study, using simultaneously recorded, multiple intracranial stereo-electroencephalographic recordings, we examined the dynamic pattern of correlation between intrinsic functional connectivity (iFC) of the AC and either bottom-up extrinsic functional connectivity (eFC) from the AC to higher-order cortices or top-down eFC from higher-order cortices toward the AC

  • Using the Talairach coordinates, all the 769 depth electrodes were located in the following brain areas: the AC (n = 61), middle frontal gyrus (MFG, n = 48), inferior frontal gyrus (IFG, n = 23), precentral gyrus (n = 64), postcentral gyrus (PoG, n = 27), inferior parietal lobule (IPL, n = 35), superior temporal gyrus (n = 26), middle temporal gyrus (MTG, n = 37), inferior temporal gyrus (ITG, n = 11), parahippocampal gyrus (ParaHipp, n = 35), insula (n = 33), cingulate gyrus (n = 72), fusiform gyrus (n = 31), and precuneus (n = 43)

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Summary

Introduction

Passive listening to sound stimuli activates both the auditory cortex (AC) and some cortical regions that do not belong to the typical auditory system (Ackermann et al, 2001; Brown et al, 2004; Londei et al, 2007). Auditory Intrinsic and Extrinsic Connectivity (STG) and the precentral gyrus (PreG) (Potes et al, 2012). These reports suggest that the AC both sends bottom-up signals to and receives top-down signals from higher-order cortical regions that underlie various auditory processes, such as speech and music perception. Investigation of the temporal dynamics of signal propagations between the AC and its connected cortical regions (even under passive listening conditions) is critical for understanding the cortical mechanism underlying auditory processing. Studies using intracranial EEG recordings in humans to examine the temporal dynamic of signal propagations between the AC and its connected cortical regions have rarely been reported

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