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Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state.

ABSTRACT: Alpha oscillations are a distinctive feature of the awake resting state of the human brain. However, their functional role in resting-state neuronal dynamics remains poorly understood. Here we show that, during resting wakefulness, alpha oscillations drive an alternation of attenuation and amplification bouts in neural activity. Our analysis indicates that inhibition is activated in pulses that last for a single alpha cycle and gradually suppress neural activity, while excitation is successively enhanced over a few alpha cycles to amplify neural activity. Furthermore, we show that long-term alpha amplitude fluctuations-the "waxing and waning" phenomenon-are an attenuation-amplification mechanism described by a power-law decay of the activity rate in the "waning" phase. Importantly, we do not observe such dynamics during non-rapid eye movement (NREM) sleep with marginal alpha oscillations. The results suggest that alpha oscillations modulate neural activity not only through pulses of inhibition (pulsed inhibition hypothesis) but also by timely enhancement of excitation (or disinhibition).

SUBMITTER: Lombardi F

PROVIDER: S-EPMC10842118 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state.

Lombardi Fabrizio F Herrmann Hans J HJ Parrino Liborio L Plenz Dietmar D Scarpetta Silvia S Vaudano Anna Elisabetta AE de Arcangelis Lucilla L Shriki Oren O

Cell reports 20230929 10

Alpha oscillations are a distinctive feature of the awake resting state of the human brain. However, their functional role in resting-state neuronal dynamics remains poorly understood. Here we show that, during resting wakefulness, alpha oscillations drive an alternation of attenuation and amplification bouts in neural activity. Our analysis indicates that inhibition is activated in pulses that last for a single alpha cycle and gradually suppress neural activity, while excitation is successively ...[more]

PMID: 37777965

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Project description:AimResting-state fMRI (rs-fMRI) is often used to infer regional brain interactions from the degree of temporal correlation between spontaneous low-frequency fluctuations, thought to reflect local changes in the BOLD signal due to neuronal activity. One complication in the analysis and interpretation of rs-fMRI data is the existence of non-neuronal low frequency physiological noise (systemic low frequency oscillations; sLFOs) which occurs within the same low frequency band as the signal used to compute functional connectivity. Here, we demonstrate the use of a time lag mapping technique to estimate and mitigate the effects of the sLFO signal on resting state functional connectivity of awake squirrel monkeys.MethodsTwelve squirrel monkeys (6 male/6 female) were acclimated to awake scanning procedures; whole-brain fMRI images were acquired with a 9.4 Tesla scanner. Rs-fMRI data was preprocessed using an in-house pipeline and sLFOs were detected using a seed regressor generated by averaging BOLD signal across all voxels in the brain, which was then refined recursively within a time window of -16-12 s. The refined regressor was then used to estimate the voxel-wise sLFOs; these regressors were subsequently included in the general linear model to remove these moving hemodynamic components from the rs-fMRI data using general linear model filtering. Group level independent component analysis (ICA) with dual regression was used to detect resting-state networks and compare networks before and after sLFO denoising.ResultsResults show sLFOs constitute ~64% of the low frequency fMRI signal in squirrel monkey gray matter; they arrive earlier in regions in proximity to the middle cerebral arteries (e.g., somatosensory cortex) and later in regions close to draining vessels (e.g., cerebellum). Dual regression results showed that the physiological noise was significantly reduced after removing sLFOs and the extent of reduction was determined by the brain region contained in the resting-state network.ConclusionThese results highlight the need to estimate and remove sLFOs from fMRI data before further analysis.

Dataset Information

Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state.

Publications

Beyond pulsed inhibition: Alpha oscillations modulate attenuation and amplification of neural activity in the awake resting state.

Similar Datasets

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