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      Neural dynamics of selective attention deficits in HIV-associated neurocognitive disorder

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          Abstract

          Objective

          To identify the neural markers of attention dysfunction in patients with HIV-associated neurocognitive disorder (HAND).

          Methods

          Sixty participants, including 40 HIV-infected adults (half with HAND) and 20 demographically matched controls performed a visual selective attention task while undergoing high-density magnetoencephalography. Neuronal activity related to selective attention processing was quantified and compared across the 3 groups, and correlated with neuropsychological measures of attention and executive function. Spontaneous neural activity was also extracted from these attention-related cortical areas and examined with respect to HAND status.

          Results

          HIV-infected participants with and without HAND exhibited behavioral selective attention deficits on the magnetoencephalography task, as indicated by an increased flanker effect. Neuronal measures of flanker interference activity in the alpha and theta range revealed differential dynamics in attention-related brain areas across the 3 groups, especially in those with HAND. In addition, theta range flanker interference activity in the left inferior frontal and dorsolateral prefrontal cortex was associated with executive function and attention composite scores, respectively. Progressively stronger spontaneous alpha and theta activity was also found in unimpaired HIV-infected and HAND participants relative to controls across brain regions implicated in different components of attention processing.

          Conclusions

          Behavioral and neuronal metrics of selective attention performance distinguish participants with HAND from controls and unimpaired HIV-infected participants. These metrics, along with measures of local spontaneous neural activity, may hold promise as early markers of cognitive decline in participants with HIV infection and be useful prognostic indicators for HAND.

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          Most cited references29

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          Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements.

          S Taulu, J Simola (2006)
          Limitations of traditional magnetoencephalography (MEG) exclude some important patient groups from MEG examinations, such as epilepsy patients with a vagus nerve stimulator, patients with magnetic particles on the head or having magnetic dental materials that cause severe movement-related artefact signals. Conventional interference rejection methods are not able to remove the artefacts originating this close to the MEG sensor array. For example, the reference array method is unable to suppress interference generated by sources closer to the sensors than the reference array, about 20-40 cm. The spatiotemporal signal space separation method proposed in this paper recognizes and removes both external interference and the artefacts produced by these nearby sources, even on the scalp. First, the basic separation into brain-related and external interference signals is accomplished with signal space separation based on sensor geometry and Maxwell's equations only. After this, the artefacts from nearby sources are extracted by a simple statistical analysis in the time domain, and projected out. Practical examples with artificial current dipoles and interference sources as well as data from real patients demonstrate that the method removes the artefacts without altering the field patterns of the brain signals.
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            Dynamic imaging of coherent sources: Studying neural interactions in the human brain.

            J. Gross, J. Kujala, M. Hämäläinen … (2001)
            Functional connectivity between cortical areas may appear as correlated time behavior of neural activity. It has been suggested that merging of separate features into a single percept ("binding") is associated with coherent gamma band activity across the cortical areas involved. Therefore, it would be of utmost interest to image cortico-cortical coherence in the working human brain. The frequency specificity and transient nature of these interactions requires time-sensitive tools such as magneto- or electroencephalography (MEG/EEG). Coherence between signals of sensors covering different scalp areas is commonly taken as a measure of functional coupling. However, this approach provides vague information on the actual cortical areas involved, owing to the complex relation between the active brain areas and the sensor recordings. We propose a solution to the crucial issue of proceeding beyond the MEG sensor level to estimate coherences between cortical areas. Dynamic imaging of coherent sources (DICS) uses a spatial filter to localize coherent brain regions and provides the time courses of their activity. Reference points for the computation of neural coupling may be based on brain areas of maximum power or other physiologically meaningful information, or they may be estimated starting from sensor coherences. The performance of DICS is evaluated with simulated data and illustrated with recordings of spontaneous activity in a healthy subject and a parkinsonian patient. Methods for estimating functional connectivities between brain areas will facilitate characterization of cortical networks involved in sensory, motor, or cognitive tasks and will allow investigation of pathological connectivities in neurological disorders.
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              HIV-associated neurocognitive disorder.

              David Clifford, Beau M Ances (2013)
              Neurological involvement in HIV is often associated with cognitive impairment. Although severe and progressive neurocognitive impairment has become rare in HIV clinics in the era of potent antiretroviral therapy, most patients with HIV worldwide have poor outcomes on formal neurocognitive tests. In this Review, we describe the manifestations of HIV-associated neurocognitive disorder in the era of effective HIV therapy, outline diagnosis and treatment recommendations, and explore the research questions that remain. Although comorbid disorders, such as hepatitis C infection or epilepsy, might cause some impairment, their prevalence is insufficient to explain the frequency with which it is encountered. HIV disease markers, such as viral load and CD4 cell counts, are not strongly associated with ongoing impairment on treatment, whereas cardiovascular disease markers and inflammatory markers are. New cerebrospinal fluid and neuroimaging biomarkers are needed to detect and follow impairment. Ongoing research efforts to optimise HIV therapy within the CNS, and potentially to intervene in downstream mechanisms of neurotoxicity, remain important avenues for future investigation. Ultimately, the full control of virus in the brain is a necessary step in the goal of HIV eradication. Copyright © 2013 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Brandon J. Lew:
                Comment :

                Scientific Advisory Boards:

                1. NONE

                Gifts:

                1. NONE

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                1. NONE

                Editorial Boards:

                1. NONE

                Patents:

                1. NONE

                Publishing Royalties:

                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. NONE

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. NONE

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

                Royalty Payments, Technology or Inventions:

                1. NONE

                Stock/Stock Options, Research Sponsor:

                1. NONE

                Stock/Stock Options, Medical Equipment & Materials:

                1. NONE

                Legal Proceedings:

                1. NONE

                Timothy J. McDermott:
                Comment :

                Scientific Advisory Boards:

                1. NONE

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                1. NONE

                Funding for Travel or Speaker Honoraria:

                1. NONE

                Editorial Boards:

                1. NONE

                Patents:

                1. NONE

                Publishing Royalties:

                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. NONE

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. NONE

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

                Royalty Payments, Technology or Inventions:

                1. NONE

                Stock/Stock Options, Research Sponsor:

                1. NONE

                Stock/Stock Options, Medical Equipment & Materials:

                1. NONE

                Legal Proceedings:

                1. NONE

                Alex I. Wiesman:
                Comment :

                Scientific Advisory Boards:

                1. NONE

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                1. NONE

                Funding for Travel or Speaker Honoraria:

                1. NONE

                Editorial Boards:

                1. NONE

                Patents:

                1. NONE

                Publishing Royalties:

                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. NONE

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. NONE

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

                Royalty Payments, Technology or Inventions:

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                1. NONE

                Legal Proceedings:

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                Jennifer O'Neill:
                Comment :

                Scientific Advisory Boards:

                1. NONE

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                1. NONE

                Funding for Travel or Speaker Honoraria:

                1. NONE

                Editorial Boards:

                1. NONE

                Patents:

                1. NONE

                Publishing Royalties:

                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. 1) ViiV Healthcare/GlaxoSmithKline; 2) Merck Pharmaceuticals

                Research Support, Government Entities:

                1. 1. National Institute of Mental Health, R01-MH103220, acquisition of data, study concept and design 2014-2019; 2. National Institute of Mental Health, R01-MH116782, acquisition of data, study concept and design, 2018-2023; 3. National Institute of Mental Health, P30-MH062261, acquisition of data, study concept and design, 2015-2022; 4. National Institute on Drug Abuse, R03-DA041917, acquisition of data, study concept and design, 2016-2019

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. NONE

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

                Royalty Payments, Technology or Inventions:

                1. NONE

                Stock/Stock Options, Research Sponsor:

                1. NONE

                Stock/Stock Options, Medical Equipment & Materials:

                1. NONE

                Legal Proceedings:

                1. NONE

                Mackenzie S. Mills:
                Comment :

                Scientific Advisory Boards:

                1. NONE

                Gifts:

                1. NONE

                Funding for Travel or Speaker Honoraria:

                1. NONE

                Editorial Boards:

                1. NONE

                Patents:

                1. NONE

                Publishing Royalties:

                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. (1) National Institute of Mental Health, R01-MH103220, participating personnel, acquisition of data, analysis of data, 2015-2017 (2) National Science Foundation, #1539067, participating personnel, acquisition of data, analysis of data, 2015-2017 Mackenzie S. Mills ? Reports no disclosures

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. (1) National Institute of Mental Health, R01-MH103220, (2) National Science Foundation, #1539067

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

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                Kevin R. Robertson:
                Comment :

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                1. viiv

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                1. NONE

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                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. NIMH, NIAID 2015-2017

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. NONE

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

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                Howard S. Fox:
                Comment :

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                1. NONE

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                Publishing Royalties:

                1. NONE

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                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. 1. NIH, R01 MH073490, PI (2005-2016) 2. NIH, R21 MH106422, multiple PI (2015-2017) 3. NIH, R01 DA032513, multiple PI (2011-2017) 4. NIH, P30 MH062261, multiple PI (2000-2020) 5. NIH, 1U54GM115458, PI Rizzo, co-I, (2016-2021) 6. NIH, 1R01DA04316, multiple PI (2016-2021) 7. NIH, 1R01DA043258, multiple PI (2011-2016) 8. NIH, 1R01AI124965, co-I (2016-2021) 9. NIH, P01 DA028555 core PI (2010-2020) 10. NIH, U24 MH100925-01, multiple PI (2013-2018) 11. NIH, R01 DA040397, multiple PI (2015-2020)

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. 1. Michael J. Fox Foundation (2016-2017)

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

                Royalty Payments, Technology or Inventions:

                1. NONE

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                1. NONE

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                1. NONE

                Legal Proceedings:

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                Susan Swindells:
                Comment :

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                1. NONE

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                1. NONE

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                1. NONE

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                1. NONE

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                1. NONE

                Publishing Royalties:

                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. NONE

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. NONE

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

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                1. NONE

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                Tony W. Wilson:
                Comment :

                Scientific Advisory Boards:

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                1. NONE

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                1. NONE

                Publishing Royalties:

                1. NONE

                Employment, Commercial Entity:

                1. NONE

                Consultancies:

                1. NONE

                Speakers' Bureaus:

                1. NONE

                Other Activities:

                1. NONE

                Clinical Procedures or Imaging Studies:

                1. NONE

                Research Support, Commercial Entities:

                1. NONE

                Research Support, Government Entities:

                1. 1. National Institute of Mental Health, R01-MH103220, PI, 2014-2019 2. National Institute of Mental Health, R01-MH116782, PI, 2018-2023 3. National Institute of Mental Health, P30-MH062261, Co- PI of Imaging Core, 2015-2022 4. National Institute on Drug Abuse, R03-DA041917, PI, 2016-2019 5. National Institute on Aging, F31-AG055332, Sponsor, 2017-2022 6. National Science Foundation, #1539067, Co-PI, 2015-2019

                Research Support, Academic Entities:

                1. NONE

                Research Support, Foundations and Societies:

                1. 1. American Heart Association, 16CSA28580000, Co-PI, 2016- 2019

                Stock/Stock Options/Board of Directors Compensation:

                1. NONE

                License Fee Payments, Technology or Inventions:

                1. NONE

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                Journal
                Journal ID (nlm-ta): Neurology
                Journal ID (iso-abbrev): Neurology
                Journal ID (hwp): neurology
                Journal ID (publisher-id): neur
                Journal ID (pmc): neurology
                Journal ID (publisher-id): NEUROLOGY
                Title: Neurology
                Publisher: Lippincott Williams & Wilkins (Hagerstown, MD )
                ISSN (Print): 0028-3878
                ISSN (Electronic): 1526-632X
                Publication date (Print): 13 November 2018
                Publication date PMC-release: 13 November 2018
                Volume: 91
                Issue: 20
                Pages: e1860-e1869
                Affiliations
                From the Departments of Neurological Sciences (B.J.L., T.J.M., A.I.W., M.S.M., T.W.W.), Internal Medicine (J.O., S.S.), and Pharmacology and Experimental Neuroscience (H.S.F.), University of Nebraska Medical Center, Omaha; and Department of Neurology (K.R.R.), University of North Carolina School of Medicine, Chapel Hill.
                Author notes
                Correspondence Dr. Wilson twwilson@ 123456unmc.edu

                Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

                The Article Processing Charge was funded by the National Institutes of Health (NIH).

                Article
                Publisher ID: NEUROLOGY2018888347
                DOI: 10.1212/WNL.0000000000006504
                PMC ID: 6260195
                PubMed ID: 30333162
                SO-VID: c9cf9c7f-eea9-4df1-b7d6-32b27e9a6fe8
                Copyright © Copyright © 2018 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND), which permits downloading and sharing the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

                History
                Date received : 26 February 2018
                Date accepted : 02 August 2018
                Funding
                Funded by: NIH
                Award ID: MH103220, MH116782, MH062261, AG055332
                Funded by: NSF
                Award ID: 1539067
                Categories
                Subject: 283
                Subject: 34
                Subject: 38
                Subject: 208
                Subject: Article
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