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Harnessing residual unconscious processing with neurofeedback to regulate visual awareness: implications for spatial attention deficits in patients with neglect after stroke

English title Harnessing residual unconscious processing with neurofeedback to regulate visual awareness: implications for spatial attention deficits in patients with neglect after stroke
Applicant Vuilleumier Patrik
Number 166704
Funding scheme Project funding (Div. I-III)
Research institution Dépt des Neurosciences Fondamentales Faculté de Médecine Université de Genève
Institution of higher education University of Geneva - GE
Main discipline Neurophysiology and Brain Research
Start/End 01.05.2016 - 31.12.2019
Approved amount 600'000.00
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All Disciplines (2)

Discipline
Neurophysiology and Brain Research
Psychology

Keywords (9)

Face processing; EEG; Neuropsychology; fMRI; Vision; Neglect syndrome; Consciousness; Neurofeedback; Neglect syndrome

Lay Summary (French)

Lead
Régulation de l'activité visualle inconsciente par neurofeedback: implications pour la rééducation du syndrome de négligence spatiale
Lay summary

La recherche en neuropsychologie et neuroimagerie a révélé que les zones visuelles sensorielles peuvent être activées sans conscience du stimulus. En revanche, la détection consciente est associée à une amplification des réponses sensorielles par le biais d'interactions avec les réseaux frontopariétaux qui contrôlent l'attention sélective.

Notre  projet se base sur ces observations, combinées avec les développements récents de techniques de neuroimagerie fonctionnelle qui permettent non seulement de mesurer des activités cérébrales inconscientes mais aussi de fournir ces mesures en temps réel pour des applications de « neurofeedback » (NF), où les sujets sont entrainés à réguler l’activité cérébrale d’une région cible. Chez des patients cérébro-lésés souffrant du syndrome de négligence spatiale, nous allons développer une procédure de NF en IRM fonctionnelle, permettant d'informer les patients sur l'activité en cours dans leur cortex occipital droit et de les entrainer ainsi à améliorer cette activité. Cette régulation pourrait conduire à une amélioration des symptômes de négligence. Une approche similaire sera également explorée à l'aide de NF en électro-encéphalographie (EEG).

 En parallèle, une étude sera menée chez des volontaires humains en bonne santé, visant à tester si la régulation par NF peut également moduler l'activité cérébrale produite par des stimuli inconsciemment vus, en utilisant une procédure de masquage pour induire une perception subliminale. Une régulation réussie de ces zones pourrait conduire à une meilleure détection visuelle des stimuli masqués lorsqu'ils sont présentés au niveau ou en dessous du seuil.

Ces travaux fourniront la première preuve que des activations cérébrales inaccessibles à la conscience peuvent être modifiées par un contrôle volontaire via le NF, et ainsi induire des changements dans la perception visuelle.

Direct link to Lay Summary Last update: 15.04.2016

Lay Summary (English)

Lead
Training of unconscious brain activity with real-time neuroimaging techniques: implications for treatment of neurological deficits after stroke
Lay summary

SUMMARY

 

Recent neuropsychological and neuroimaging research has revealed that sensory visual areas can be activated without conscious awareness of the eliciting stimulus. In contrast, conscious detection is associated with an amplification of sensory responses through interactions with fronto-parietal networks controlling attention and goal-oriented behavior.

 

The current project will build on these observations, combined with recent developments in functional neuroimaging techniques that allow not only measuring unconscious brain activity but also provide the opportunity to use such measure in real-time for neurofeedback (NFB) application. In brain-damaged patients with spatial neglect, we will design a novel NFB procedure with fMRI enabling us to inform patients about ongoing activity in their right occipital cortex and train them to up-regulate this activity across several weekly sessions. We predict that achieving voluntary control over right occipital activity through real-time fMRI feedback will help restore functional top-down connectivity between the intact right visual areas and the disrupted attentional systems, and thus lead to an improvement in neglect symptoms. A similar approach will also be explored using NFB with electro-encephalography (EEG) instead of fMRI to measure visual brain activity.

 A parallel investigation will be carried out in healthy human volunteers, to test whether NFB regulation can also operate on brain activity produced by unconsciously seen stimuli, using a masking procedure to induce subliminal processing. We predict that successful up-regulation of these areas may lead to improved visual detection of masked stimuli when presented at or below threshold..

 This work will provide the first evidence that brain processes unavailable to conscious awareness can be modified by voluntary control through NFB, and thus lead to subsequent changes in visual perception.

 

 

 

Direct link to Lay Summary Last update: 15.04.2016

Responsible applicant and co-applicants

Employees

Publications

Publication
Rightward exogenous attentional shifts impair perceptual memory of spatial locations in patients with left unilateral spatial neglect
Saj Arnaud, Pierce Jordan, Caroli Alice, Ronchi Roberta, Thomasson Marine, Vuilleumier Patrik (2020), Rightward exogenous attentional shifts impair perceptual memory of spatial locations in patients with left unilateral spatial neglect, in Cortex, 122, 187-197.
Differential parietal activations for spatial remapping and saccadic control in a visual memory task
Pierce Jordan E., Saj Arnaud, Vuilleumier Patrik (2019), Differential parietal activations for spatial remapping and saccadic control in a visual memory task, in Neuropsychologia.
No time for drifting: Comparing performance and applicability of signal detrending algorithms for real-time fMRI
Kopel R., Sladky R., Laub P., Koush Y., Robineau F., Hutton C., Weiskopf N., Vuilleumier P., Van De Ville D., Scharnowski F. (2019), No time for drifting: Comparing performance and applicability of signal detrending algorithms for real-time fMRI, in NeuroImage, 191, 421-429.
Disruption of large-scale electrophysiological networks in stroke patients with visuospatial neglect
RosTomas, MichelaAbele, MeyerAnais, BellmannAnne, VuadensPhilippe, ZermattenVictorine, SajArnaud, vuilleumierpatrik (2019), Disruption of large-scale electrophysiological networks in stroke patients with visuospatial neglect, in biorxiv.org, 602318.
Brain networks for engaging oneself in positive-social emotion regulation
Koush Yury, Pichon Swann, Eickhoff Simon B., Van De Ville Dimitri, Vuilleumier Patrik, Scharnowski Frank (2019), Brain networks for engaging oneself in positive-social emotion regulation, in NeuroImage, 189, 106-115.
Value-driven attentional capture in neglect
Bourgeois Alexia, Saj Arnaud, Vuilleumier Patrik (2018), Value-driven attentional capture in neglect, in Cortex, 109, 260-271.
Cross-modal integration during value-driven attentional capture
Sanz Leandro R.D., Vuilleumier Patrik, Bourgeois Alexia (2018), Cross-modal integration during value-driven attentional capture, in Neuropsychologia, 120, 105-112.
Dissociable components of spatial neglect associated with frontal and parietal lesions
Saj Arnaud, Verdon Vincent, Hauert Claude-Alain, Vuilleumier Patrik (2018), Dissociable components of spatial neglect associated with frontal and parietal lesions, in Neuropsychologia, 115, 60-69.
Effect of a single early EEG neurofeedback training on remediation of spatial neglect in the acute phase
Saj Arnaud, Ros Tomas, Michela Abele, Vuilleumier Patrik (2018), Effect of a single early EEG neurofeedback training on remediation of spatial neglect in the acute phase, in Annals of Physical and Rehabilitation Medicine, 61(2), 111-112.
Using real-time fMRI neurofeedback to restore right occipital cortex activity in patients with left visuo-spatial neglect: proof-of-principle and preliminary results
Robineau Fabien, Saj Arnaud, Neveu Rémi, Van De Ville Dimitri, Scharnowski Frank, Vuilleumier Patrik (2017), Using real-time fMRI neurofeedback to restore right occipital cortex activity in patients with left visuo-spatial neglect: proof-of-principle and preliminary results, in Neuropsychological Rehabilitation, 29(3), 339-360.
Maintenance of Voluntary Self-regulation Learned through Real-Time fMRI Neurofeedback
Robineau Fabien, Meskaldji Djalel E., Koush Yury, Rieger Sebastian W., Mermoud Christophe, Morgenthaler Stephan, Van De Ville Dimitri, Vuilleumier Patrik, Scharnowski Frank (2017), Maintenance of Voluntary Self-regulation Learned through Real-Time fMRI Neurofeedback, in Frontiers in Human Neuroscience, 11, 1-8.
Learning Control Over Emotion Networks Through Connectivity-Based Neurofeedback
Koush Yury, Meskaldji Djalel-E., Pichon Swann, Rey Gwladys, Rieger Sebastian W., Linden David E.J., Van De Ville Dimitri, Vuilleumier Patrik, Scharnowski Frank (2017), Learning Control Over Emotion Networks Through Connectivity-Based Neurofeedback, in Cerebral Cortex, bhv311-bhv311.
Increased Alpha-Rhythm Dynamic Range Promotes Recovery from Visuospatial Neglect: A Neurofeedback Study
Ros Tomas, Michela Abele, Bellman Anne, Vuadens Philippe, Saj Arnaud, Vuilleumier Patrik (2017), Increased Alpha-Rhythm Dynamic Range Promotes Recovery from Visuospatial Neglect: A Neurofeedback Study, in Neural Plasticity, 2017, 1-9.

Collaboration

Group / person Country
Types of collaboration
Philippe Vuadens Switzerland (Europe)
- Publication
- Research Infrastructure
Frederic Assal Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Frank Scharnowski Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Dimitri van de Ville Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Ranganatha Sitaram United States of America (North America)
- in-depth/constructive exchanges on approaches, methods or results

Awards

Title Year
Best poster prize. International conference on neurofeedback, Maastricht, December 2019 Title: "Regulating subliminal neural activity in thefusiform face area: a fMRI-based neurofeedback study" (presented by Lucas Peek; https://www.rtfin2019.org/107020/wiki/486308/schedule : no 14) Results unpublished, paper in preparation. Abstract: https://www.aanmelder.nl/i/doc/e3cc914da63c165edc33e24474b4eddf?forcedownload=True 2019

Associated projects

Number Title Start Funding scheme
192792 Understanding the Neural Substrates of Neurofeeback Modulations of Visual Attention: Multimodal Brain Imaging and Application to Hemispatial Neglect Syndrome 01.06.2020 Project funding (Div. I-III)
192792 Understanding the Neural Substrates of Neurofeeback Modulations of Visual Attention: Multimodal Brain Imaging and Application to Hemispatial Neglect Syndrome 01.06.2020 Project funding (Div. I-III)
114014 Functional neuroanatomy of spatial cognition and neglect syndrome after stroke 01.10.2006 Project funding (Div. I-III)

Abstract

Neuropsychological and neuroimaging research (including our own) has consistently shown that sensory visual cortical areas can be activated without conscious awareness of the eliciting stimulus. In contrast, conscious detection is associated with an amplification of sensory responses through interactions with fronto-parietal networks controlling attention and goal-oriented behavior.Thus, in patients with left spatial neglect after right hemisphere stroke, intact regions in striate and extrastriate occipital cortex still exhibit residual responses to left visual stimuli, but these remain weak and short-lived due to losses in top-down modulation from fronto-parietal areas; hence they are insufficient to give rise to conscious perception. Furthermore, in the presence of right fronto-parietal damage, even central or bilateral visual stimuli tend to produce asymmetric responses along the anatomically intact right visual pathways, with a progressive attenuation from early to higher stages of processing, eventually leading to a suppression of left visual inputs from conscious visual awareness. The current project will exploit these observations, combined with recent developments in functional neuroimaging that allow not only measuring unconscious brain activity but also provide the opportunity to use such measure in real-time for neurofeedback (NFB) application. In the first part of the project, we will design a novel NFB procedure with fMRI enabling us to inform patients about ongoing activity in their right occipital cortex and train them to up-regulate this activity across several weekly sessions. We predict that achieving voluntary control over right occipital activity through real-time fMRI feedback will help restore functional top-down connectivity between the intact right visual areas and the disrupted attentional systems, and thus lead to an improvement in neglect symptoms in both short-term (after NFB sessions) and long-term (at 6 month follow-up). No such improvement should occur after standard rehabilitation only, without NFB.Impaired visual processing in neglect patients subsequent to lesions in attentional networks is also reflected by anomalies in ongoing rhythmic oscillations in EEG recordings. In particular, asymmetries in the alpha band (8-12Hz) over posterior brain areas correlate with neglect severity in patients, in keeping with observations in healthy people that transient reduction (desynchronization) of posterior alpha activity are associated with more efficient orienting to the contralateral field and enhanced detection of a subsequent visual stimuli on the contralateral side. In a second part of the project, we will therefore use EEG neurofeedback to train patients with left neglect to suppress alpha activity over their right visual areas. EEG provides anatomically less precise information about the exact locus of training but has the advantage of reflecting activity of distributed networks, and of being easier and cheaper to perform than fMRI for potential clinical applications. We predict that successful down-regulation of right parietal alpha activity will lead to improved performance in neglect tests and reduced asymmetries in ongoing oscillations after NFB, not seen in patients with standard rehabilitation without NFB.Similar to findings in neglect, research in healthy people indicate that briefly presented stimuli in masking paradigms can evoke subliminal activation in specific visual areas, although they are not consciously seen by the subject. However, emotionally significant stimuli can boost these subliminal sensory responses, even without attention or awareness, through distinct top-down modulatory influences from emotional circuits such as the amygdala. These effects, independent from top-down modulation by fronto-parietal areas, may promote quicker access of emotional stimuli to awareness as compared with neutral stimuli. In a third part of the project, we will use a similar NFB procedure with fMRI to train healthy volunteers to regulate brain responses evoked by subliminal faces presented in a backward masking paradigm. Three different groups will be trained to regulate the face-sensitive area in fusiform cortex, the amygdala, or posterior parietal areas implicated in top-down attention, respectively, allowing us to compare the effect of NFB training on visual responses driven by bottom-up (fusiform), top-down (parietal), or both bottom-up and top-down signals (amygdala). We predict that successful up-regulation of these areas will lead to improved visual detection of masked faces, and concomitant changes in functional brain connectivity of visual areas with fronto-parietal networks, not seen in a control group receiving sham NFB.Together, these studies will provide the first evidence that brain processes unavailable to conscious awareness can be modified by voluntary control through NFB, and thus lead to subsequent changes in visual perception, opening new avenues for innovative rehabilitation strategies in neurological or psychiatric patients.
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