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Brain oscillatory dynamics in the bottom-up/top-down balance of attention – DISTRACTEDBRAINOSCI

Brain oscillatory dynamics in the bottom-up/top-down balance of attention

This project aims at testing the hypothesis that distinct oscillatory networks support bottom-up<br />and top-down attention, and at exploring the dynamic interplay between these networks, in the<br />healthy or pathological human brain.<br />

The balance between top-down and bottom-up attention

Attention improves the processing of specific information while other stimuli are disregarded. Attention operates via both top-down and bottom-up processes. Top-down attention enables the efficient performance of an on-going task by selecting the relevant information. One’s attention can however be involuntarily captured by an unexpected salient stimulus. This bottom-up form of attention is necessary to be aware of potentially important events that are nonetheless irrelevant to the on-going task (e.g. fire alarm). A good balance between bottom-up and top-down mechanisms is crucial to be both task-efficient and aware of our environment. This precarious balance is often affected in neurological and psychiatric disorders leading to increased distractibility. Despite the obvious importance of distractibility in assessing the patients’ neurological status, no index of this process has been validated in clinical practice. <br />Only few neuroimaging studies have investigated the bottom-up/top-down attention balance. Functional Magnetic Resonance Imaging works have shown that top-down and bottom-up mechanisms are supported by partially overlapping brain networks: the dorsal top-down network (parietal and posterior frontal cortices), and the ventral bottom-up network (temporo-parietal and ventral frontal regions), with the main overlap in the lateral prefrontal cortex. An oscillatory hierarchy operating across multiple spatial and temporal scales has been proposed to regulate short- and long-range communication in the brain. The investigation of this oscillatory hierarchy seems to be particularly relevant to understand the interaction between the ventral and dorsal networks and the competition between bottom-up and top-down mechanisms of attention.<br />This project aims at testing the hypothesis that distinct oscillatory networks support bottom-up and top-down attention, and at exploring the dynamic interplay between these networks, in the healthy or pathological human brain.

To achieve this aim, we propose a new paradigm in the auditory modality that will enable to investigate both bottom-up and top-down attention mechanisms, at the same time: the Competitive Attention Test. We will explore brain activity and connectivity during this test using simultaneous multi-level functional brain recordings – scalp electroencephalography (EEG), intracortical EEG, and magnetoencephalography (MEG) – combined with anatomical measures and advanced signal analysis methods.
First, the typical dynamic oscillatory interaction between the bottom-up and top-down attention networks will be investigated using scalp EEG, intracortical EEG, and MEG.
Second, we will examine, using EEG and MEG measures, how the precarious equilibrium between bottom-up and top-down mechanisms of attention can be knocked off balance and lead to atypical attention functions in two pathologies: migraine and frontal stroke. An impairment of frontal attention-related networks has indeed been reported in these diseases.

So far, this project shows that top-down anticipatory attention is a dynamic process supported by a balance between facilitatory and inhibitory mechanisms according to the relevant stimuli at hand. This balance seems to be supported by different sub-bands of alpha oscillatory activity.

Moreover, we found that patients with migraine present exacerbated bottom-up and top-down attentional processes which could account for their sensory hypersensitivity.

This project will provide new insights into the brain dynamics supporting the bottom-up/top-down attention balance. It will enable the optimization of novel distractibility tests as diagnostic tools for precise characterization of attention deficits, and the development of new therapeutic tools based in particular on neurofeedback training of attention mechanisms.

Hirel C, Nighoghossian N, Lévêque Y, Hannoun S, Fornoni L, Daligault S, Bouchet P, Jung J, Tillmann B, Caclin A. Verbal and musical short-term memory: Variety of auditory disorders after stroke. Brain Cogn. 2017, 113:10-22.
doi: 10.1016/j.bandc.2017.01.003. Epub 2017 Jan 11.

Tillmann B., Hirel C., Lévêque Y. & Caclin A. (in press). Musical connections: Music perception and neurological deficits. Routledge Companion to Music Cognition. Editeurs: R. Ashley & R. Timmers. Routledge.

H A ElShafei, R Bouet, O Bertrand, A Bidet-Caulet. On the edge of your eats: Investigating the neural correlates of auditory anticipatory attention. Advances and Perspectives in Auditory Neuroscience (APAN), Satellite Symposium at the Society for Neuroscience Annual Meeting. San Diego, November 11, 2016.

Attention improves the processing of specific information while other stimuli are disregarded. Attention operates via both top-down and bottom-up processes. Top-down attention enables the efficient performance of an on-going task by selecting the relevant information. One’s attention can however be involuntarily captured by an unexpected salient stimulus and thus diverted from the previously on-going task. This bottom-up form of attention is necessary to be aware of potentially important events that are nonetheless irrelevant to the on-going task (e.g. fire alarm). A good balance between bottom-up and top-down mechanisms is crucial to be both task-efficient and aware of our environment. This precarious balance is often affected in neurological and psychiatric disorders leading to increased distractibility. Despite the obvious importance of distractibility in assessing the patients’ neurological status, no index of this process has been validated in clinical practice. Currently available tests are only suitable for revealing impairment in top-down attention, but fail to evidence any dysfunction in bottom-up attentional capture.
Only few neuroimaging studies have investigated the bottom-up/top-down attention balance. Functional Magnetic Resonance Imaging works have shown that top-down and bottom-up mechanisms are supported by partially overlapping brain networks: the dorsal top-down network (parietal and posterior frontal cortices), and the ventral bottom-up network (temporo-parietal and ventral frontal regions), with the main overlap in the lateral prefrontal cortex. An oscillatory hierarchy operating across multiple spatial and temporal scales has been proposed to regulate short- and long-range communication in the brain. The investigation of this oscillatory hierarchy seems to be particularly relevant to understand the interaction between the ventral and dorsal networks and the competition between bottom-up and top-down mechanisms of attention.
This project aims at testing the hypothesis that distinct oscillatory networks support bottom-up and top-down attention, and at exploring the dynamic interplay between these networks, in the healthy or pathological human brain.
To achieve this aim, we propose a new paradigm in the auditory modality that will enable to investigate both bottom-up and top-down attention mechanisms, at the same time: the Competitive Attention Test. We will explore brain activity and connectivity during this test using simultaneous multi-level functional brain recordings – scalp electroencephalography (EEG), intracortical EEG, and magnetoencephalography (MEG) – combined with anatomical measures and advanced signal analysis methods.
First, the typical dynamic oscillatory interaction between the bottom-up and top-down attention networks will be investigated using scalp EEG, intracortical EEG, and MEG.
Second, we will examine, using EEG and MEG measures, how the precarious equilibrium between bottom-up and top-down mechanisms of attention can be knocked off balance and lead to atypical attention functions in two pathologies: migraine and frontal stroke. An impairment of frontal attention-related networks has indeed been reported in these diseases.
This project will provide new insights into the brain dynamics supporting the bottom-up/top-down attention balance. It will enable the optimization of novel distractibility tests as diagnostic tools for precise characterization of attention deficits, and the development of new therapeutic tools based in particular on neurofeedback training of attention mechanisms.

Project coordinator

Madame Aurélie BIDET-CAULET (Centre de Recherche en Neurosciences de Lyon, INSERM U1028-CNRS UMR5292)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.

Partner

CRNL Centre de Recherche en Neurosciences de Lyon, INSERM U1028-CNRS UMR5292

Help of the ANR 391,716 euros
Beginning and duration of the scientific project: September 2014 - 48 Months

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