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Loss of interplay: Frontoparietal dynamics underlie working memory deficits in multiple sclerosis

View ORCID ProfileAlejandra Figueroa-Vargas, Claudia Cárcamo, View ORCID ProfileRodrigo Henríquez, View ORCID ProfileFrancisco Zamorano, Ethel Ciampi, Reinaldo Uribe, Vásquez Macarena, Francisco Aboitiz, View ORCID ProfilePablo Billeke
doi: https://doi.org/10.1101/639930
Alejandra Figueroa-Vargas
Laboratorio de Neurociencia Social y Neuromodulación, Centro de Investigación en Complejidad Social (neuroCICS), Universidad del Desarrollo, Santiago de Chile
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  • ORCID record for Alejandra Figueroa-Vargas
  • For correspondence: amfigueroa@udd.cl pbilleke@udd.cl
Claudia Cárcamo
Departamento de Neurología, Hospital Clínico de la Pontificia Universidad Católica de Chile
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Rodrigo Henríquez
Departamento de Psiquiatría, Escuela de Medicina, and Centro Interdisciplinario de Neurociencias, Pontificia Universidad Católica de Chile
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  • ORCID record for Rodrigo Henríquez
Francisco Zamorano
Laboratorio de Neurociencia Social y Neuromodulación, Centro de Investigación en Complejidad Social (neuroCICS), Universidad del Desarrollo, Santiago de Chile
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Ethel Ciampi
Departamento de Neurología, Hospital Clínico de la Pontificia Universidad Católica de ChileServicio de Neurología, Hospital Dr. Sótero del Río, Santiago de Chile
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Reinaldo Uribe
Departamento de Neurología, Hospital Clínico de la Pontificia Universidad Católica de ChileServicio de Neurología, Hospital Dr. Sótero del Río, Santiago de Chile
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Vásquez Macarena
Departamento de Neurología, Hospital Clínico de la Pontificia Universidad Católica de Chile
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Francisco Aboitiz
Departamento de Psiquiatría, Escuela de Medicina, and Centro Interdisciplinario de Neurociencias, Pontificia Universidad Católica de Chile
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Pablo Billeke
Laboratorio de Neurociencia Social y Neuromodulación, Centro de Investigación en Complejidad Social (neuroCICS), Universidad del Desarrollo, Santiago de Chile
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  • For correspondence: amfigueroa@udd.cl pbilleke@udd.cl
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Abstract

Multiple sclerosis is a chronic demyelinating disease of the central nervous system that provokes motor, cognitive and neuropsychiatric symptoms. Cognitive symptoms are a core feature of the disease, affecting everyday life functioning in 40 to 70% of patients. Working Memory impairment is one of the most common cognitive deficits, crucially affecting goal-directed behavior. However, evidence of the neurobiological mechanisms underlying these impairments is scarce. To address this issue, we investigated a working memory task concomitantly with electroencephalographic records in twenty patients with relapsing-remitting multiple sclerosis who had minimal clinical cognitive alteration, and in twenty healthy control subjects. Participants first watched a memory set of two, four, or six consonants that had to be memorized and, after a black screen that was shown for two seconds, a target stimulus was displayed. We correlated both time-frequency and functional brain connectivity with memory load and behavioral performance. We found that patients and healthy controls presented similar accuracy rates. For high memory loads, patients demonstrated longer reaction times for incorrect responses when the probe was part of the memory set, revealing an increase in cognitive effort. We then evaluated the single trial correlation between the power of the oscillatory activity and the memory load. The healthy control group showed an increase of left frontal and parietal theta activity, while the patient group did not show this increase. The analysis of the successful memory performances demonstrated that controls presented a greater medial theta activity during the maintenance stage; whereas, the patient group showed a decrease in this activity. Interestingly, cortical connectivity analyses using Granger Causality revealed that healthy controls presented a load-modulated progression of the frontal-to-parietal connectivity that indicated successful memory performance, while the patients did not show this pattern. Consistently, phase-amplitude coupling analyses showed that this connectivity was carried out by frontal delta/theta phase to parietal gamma amplitude modulation. Frontal-to-parietal connectivity correlated with working memory capacity in patients measure by Paced Auditory Serial Addition Test. These results indicate that patients with multiple sclerosis present alterations in their capacity to sustain oscillatory dynamics that maintain information in working memory. Thus, differences in brain oscillations and connectivity could be useful for early detection and to study working memory alterations in multiple sclerosis, as well as to implement new therapeutic interventions using non-invasive brain stimulation.

  • Abbreviations

    BVMT-R
    Brief Visuospatial Memory Test-Revised
    CBP
    Cluster-based permutation
    CCC
    Circular Correlation Coefficient
    CSD
    Current Source Density
    CVLT-VII
    California Verbal Learning Test
    EDSS
    Expanded Disability Status Scale
    GC
    Granger Causality
    GLM
    General Linear Model
    ICA
    Independent Component Analysis
    PAC
    Phase-amplitude Coupling
    PASAT
    Paced Auditory Serial Addition Test
    PFC
    prefrontal cortex
    RR
    relapsing-remitting
    RT
    Reaction Time
    SDMT
    Symbol Digit Modalities Test
    WM
    Working Memory
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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    Posted May 17, 2019.
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    Loss of interplay: Frontoparietal dynamics underlie working memory deficits in multiple sclerosis
    Alejandra Figueroa-Vargas, Claudia Cárcamo, Rodrigo Henríquez, Francisco Zamorano, Ethel Ciampi, Reinaldo Uribe, Vásquez Macarena, Francisco Aboitiz, Pablo Billeke
    bioRxiv 639930; doi: https://doi.org/10.1101/639930
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    Loss of interplay: Frontoparietal dynamics underlie working memory deficits in multiple sclerosis
    Alejandra Figueroa-Vargas, Claudia Cárcamo, Rodrigo Henríquez, Francisco Zamorano, Ethel Ciampi, Reinaldo Uribe, Vásquez Macarena, Francisco Aboitiz, Pablo Billeke
    bioRxiv 639930; doi: https://doi.org/10.1101/639930

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