Convergent and Divergent Oscillatory Aberrations During Visuospatial Processing in HIV-related Cognitive Impairment and Alzheimer's Disease

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2022 Jul 20

PMID 35855581

Authors

Chloe E Meehan

Christine M Embury

Alex I Wiesman

Mikki Schantell

Sara L Wolfson

Jennifer ONeill

Susan Swindells

Craig M Johnson

Pamela E May

Daniel L Murman

Tony W Wilson

Affiliations

Soon will be listed here.

Abstract

Adults with HIV frequently develop a form of mild cognitive impairment known as HIV-associated neurocognitive disorder (HAND), but presumably cognitive decline in older persons with HIV could also be attributable to Alzheimer's disease (AD). However, distinguishing these two conditions in individual patients is exceedingly difficult, as the distinct neural and neuropsychological features are poorly understood and most studies to date have only investigated HAND or AD spectrum (ADS) disorders in isolation. The current study examined the neural dynamics underlying visuospatial processing using magnetoencephalography (MEG) in 31 biomarker-confirmed patients on the ADS, 26 older participants who met criteria for HAND, and 31 older cognitively normal controls. MEG data were examined in the time-frequency domain, and a data-driven approach was utilized to identify the neural dynamics underlying visuospatial processing. Both clinical groups (ADS/HAND) were significantly less accurate than controls on the task and exhibited stronger prefrontal theta oscillations compared to controls. Regarding disease-specific alterations, those with HAND exhibited stronger alpha oscillations than those on the ADS in frontoparietal and temporal cortices. These results indicate both common and unique neurophysiological alterations among those with ADS disorders and HAND in regions serving visuospatial processing and suggest the underlying neuropathological features are at least partially distinct.

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References

Doesburg S, Bedo N, Ward L . Top-down alpha oscillatory network interactions during visuospatial attention orienting. Neuroimage. 2016; 132:512-519. DOI: 10.1016/j.neuroimage.2016.02.076. View

Namagga J, Rukundo G, Voss J . Prevalence and Risk Factors of HIV-Associated Neurocognitive Disorders in Rural Southwestern Uganda. J Assoc Nurses AIDS Care. 2019; 30(5):531-538. PMC: 6716529. DOI: 10.1097/JNC.0000000000000036. View

Hillebrand A, Barnes G . A quantitative assessment of the sensitivity of whole-head MEG to activity in the adult human cortex. Neuroimage. 2002; 16(3 Pt 1):638-50. DOI: 10.1006/nimg.2002.1102. View

Israel S, Hassanzadeh-Behbahani S, Turkeltaub P, Moore D, Ellis R, Jiang X . Different roles of frontal versus striatal atrophy in HIV-associated neurocognitive disorders. Hum Brain Mapp. 2019; 40(10):3010-3026. PMC: 6865775. DOI: 10.1002/hbm.24577. View

Robertson K, Smurzynski M, Parsons T, Wu K, Bosch R, Wu J . The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS. 2007; 21(14):1915-21. DOI: 10.1097/QAD.0b013e32828e4e27. View

Beauchamp M . See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex. Curr Opin Neurobiol. 2005; 15(2):145-53. DOI: 10.1016/j.conb.2005.03.011. View

Maris E, Oostenveld R . Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods. 2007; 164(1):177-90. DOI: 10.1016/j.jneumeth.2007.03.024. View

Falchier A, Clavagnier S, Barone P, Kennedy H . Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci. 2002; 22(13):5749-59. PMC: 6758216. DOI: 20026562. View

Mohamed M, Skolasky R, Zhou Y, Ye W, Brasic J, Brown A . Beta-amyloid (Aβ) uptake by PET imaging in older HIV+ and HIV- individuals. J Neurovirol. 2020; 26(3):382-390. DOI: 10.1007/s13365-020-00836-1. View

10.

Kovach C, Gander P . The demodulated band transform. J Neurosci Methods. 2015; 261:135-54. PMC: 5084918. DOI: 10.1016/j.jneumeth.2015.12.004. View

11.

Rubin L, Sundermann E, Moore D . The current understanding of overlap between characteristics of HIV-associated neurocognitive disorders and Alzheimer's disease. J Neurovirol. 2019; 25(5):661-672. PMC: 6646104. DOI: 10.1007/s13365-018-0702-9. View

12.

Thiyagesh S, Farrow T, Parks R, Accosta-Mesa H, Young C, Wilkinson I . The neural basis of visuospatial perception in Alzheimer's disease and healthy elderly comparison subjects: an fMRI study. Psychiatry Res. 2009; 172(2):109-16. DOI: 10.1016/j.pscychresns.2008.11.002. View

13.

Wiesman A, Wilson T . The impact of age and sex on the oscillatory dynamics of visuospatial processing. Neuroimage. 2018; 185:513-520. PMC: 6290353. DOI: 10.1016/j.neuroimage.2018.10.036. View

14.

Chang L, Speck O, Miller E, Braun J, Jovicich J, Koch C . Neural correlates of attention and working memory deficits in HIV patients. Neurology. 2001; 57(6):1001-7. DOI: 10.1212/wnl.57.6.1001. View

15.

Folstein M, Folstein S, McHugh P . "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975; 12(3):189-98. DOI: 10.1016/0022-3956(75)90026-6. View

16.

Pfeffer R, Kurosaki T, Harrah Jr C, Chance J, Filos S . Measurement of functional activities in older adults in the community. J Gerontol. 1982; 37(3):323-9. DOI: 10.1093/geronj/37.3.323. View

17.

Barton B, Brewer A . Visual Field Map Clusters in High-Order Visual Processing: Organization of V3A/V3B and a New Cloverleaf Cluster in the Posterior Superior Temporal Sulcus. Front Integr Neurosci. 2017; 11:4. PMC: 5329644. DOI: 10.3389/fnint.2017.00004. View

18.

Hillebrand A, Singh K, Holliday I, Furlong P, Barnes G . A new approach to neuroimaging with magnetoencephalography. Hum Brain Mapp. 2005; 25(2):199-211. PMC: 6871673. DOI: 10.1002/hbm.20102. View

19.

Joshi A, Pontecorvo M, Clark C, Carpenter A, Jennings D, Sadowsky C . Performance characteristics of amyloid PET with florbetapir F 18 in patients with alzheimer's disease and cognitively normal subjects. J Nucl Med. 2012; 53(3):378-84. DOI: 10.2967/jnumed.111.090340. View

20.

Taulu S, Simola J . Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements. Phys Med Biol. 2006; 51(7):1759-68. DOI: 10.1088/0031-9155/51/7/008. View