Distinct roles of forward and backward alpha-band waves in spatial visual attention
- CNRS, UMR5549, France
- CerCo - CNRS, France
Abstract
Previous research has associated alpha-band [8-12Hz] oscillations with inhibitory functions: for instance, several studies showed that visual attention increases alpha-band power in the hemisphere ipsilateral to the attended location. However, other studies demonstrated that alpha oscillations positively correlate with visual perception, hinting at different processes underlying their dynamics. Here, using an approach based on traveling waves, we demonstrate that there are two functionally distinct alpha-band oscillations propagating in different directions. We analyzed EEG recordings from three datasets of human participants performing a covert visual attention task (one new dataset with N=16, two previously published datasets with N=16 and N=31). Participants were instructed to detect a brief target by covertly attending to the screen's left or right side. Our analysis reveals two distinct processes: allocating attention to one hemifield increases top-down alpha-band waves propagating from frontal to occipital regions ipsilateral to the attended location, both with or without visual stimulation. These top-down oscillatory waves correlate positively with alpha-band power in frontal and occipital regions. Yet, different alpha-band waves propagate from occipital to frontal regions and contralateral to the attended location. Crucially, these forward waves were present only during visual stimulation, suggesting a separate mechanism related to visual processing. Together, these results reveal two distinct processes reflected by different propagation directions, demonstrating the importance of considering oscillations as traveling waves when characterizing their functional role.
Data availability
Three datasets have been analyzed in this study and all of them are available from the Open Science Framework (as specified in the 'Methods/Participants' section). Code to analyze the data is available here: https://github.com/artipago/Travelling-waves-EEG-2.0, as specified in the 'Methods/Statistical analysis' section
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Distinct roles of forward and backward alpha-band waves in spatial visual attentionOSF, DOI: https://osf.io/PN784/.
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Alpha-Band Oscillations Enable Spatially and Temporally Resolved Tracking of Covert Spatial AttentionOSF, https://doi.org/10.17605/OSF.IO/M64UE.
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Neural Evidence for the Contribution of Active Suppression During Working Memory FilteringOSF, https://doi.org/10.1093/cercor/bhx336.
Article and author information
Author details
Funding
European Research Council (101075930)
- Andrea Alamia
Agence Nationale de la Recherche (ANR-19-PI3A-0004)
- Rufin VanRullen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: This study adheres to the guidelines for research at the "Centre de Recherche Cerveau et Cognition," and the protocol was approved by the local ethical committee "Commité de protection des Personnes Sud Méditerranée 1" (ethics approval number N˚ 2019-A02641-56).
Copyright
© 2023, Alamia et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Distinct roles of forward and backward alpha-band waves in spatial visual attention
eLife 12:e85035.
https://doi.org/10.7554/eLife.85035
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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Human-specific cognitive abilities depend on information processing in the cerebral cortex, where the neurons are significantly larger and their processes longer and sparser compared to rodents. We found that, in synaptically connected layer 2/3 pyramidal cells (L2/3 PCs), the delay in signal propagation from soma to soma is similar in humans and rodents. To compensate for the longer processes of neurons, membrane potential changes in human axons and/or dendrites must propagate faster. Axonal and dendritic recordings show that the propagation speed of action potentials (APs) is similar in human and rat axons, but the forward propagation of excitatory postsynaptic potentials (EPSPs) and the backward propagation of APs are 26 and 47% faster in human dendrites, respectively. Experimentally-based detailed biophysical models have shown that the key factor responsible for the accelerated EPSP propagation in human cortical dendrites is the large conductance load imposed at the soma by the large basal dendritic tree. Additionally, larger dendritic diameters and differences in cable and ion channel properties in humans contribute to enhanced signal propagation. Our integrative experimental and modeling study provides new insights into the scaling rules that help maintain information processing speed albeit the large and sparse neurons in the human cortex.
