Altered visual entrainment in patients with Alzheimer’s disease: magnetoencephalography evidence

Seth D Springer; Alex I Wiesman; Pamela E May; Mikki Schantell; Hallie J Johnson; Madelyn P Willett; Camilo A Castelblanco; Jacob A Eastman; Nicholas J Christopher-Hayes; Sara L Wolfson; Craig M Johnson; Daniel L Murman; Tony W Wilson

doi:10.1093/braincomms/fcac198

journal article Open Access Jul 04, 2022

Altered visual entrainment in patients with Alzheimer’s disease: magnetoencephalography evidence

Seth D Springer

Alex I Wiesman Pamela E May Mikki Schantell

Hallie J Johnson Madelyn P Willett Camilo A Castelblanco

Jacob A Eastman Nicholas J Christopher-Hayes Sara L Wolfson

Craig M Johnson Daniel L Murman Tony W Wilson

Brain Communications Vol. 4 No. 4 · Oxford University Press (OUP)

View at Publisher Save 10.1093/braincomms/fcac198

Abstract

AbstractRecent research has indicated that rhythmic visual entrainment may be useful in clearing pathological protein deposits in the central nervous system of mouse models of Alzheimer’s disease. However, visual entrainment studies in human patients with Alzheimer’s disease are rare, and as such the degree to which these patients exhibit aberrations in the neural tracking of rhythmic visual stimuli is unknown. To fill this gap, we recorded magnetoencephalography during a 15 Hz visual entrainment paradigm in amyloid-positive patients on the Alzheimer’s disease spectrum and compared their neural responses to a demographically matched group of biomarker-negative healthy controls. Magnetoencephalography data were imaged using a beamformer and virtual sensor data were extracted from the peak visual entrainment responses. Our results indicated that, relative to healthy controls, participants on the Alzheimer’s disease spectrum exhibited significantly stronger 15 Hz entrainment in primary visual cortices relative to a pre-stimulus baseline period. However, the two groups exhibited comparable absolute levels of neural entrainment, and higher absolute levels of entertainment predicted greater Mini-mental Status Examination scores, such that those patients whose absolute entrainment amplitude was closer to the level seen in controls had better cognitive function. In addition, 15 Hz periodic activity, but not aperiodic activity, during the pre-stimulus baseline period was significantly decreased in patients on the Alzheimer’s disease spectrum. This pattern of results indicates that patients on the Alzheimer’s disease spectrum exhibited increased visual entrainment to rhythmic stimuli and that this increase is likely compensatory in nature. More broadly, these results show that visual entrainment is altered in patients with Alzheimer’s disease and should be further examined in future studies, as changes in the capacity to entrain visual stimuli may prove useful as a marker of Alzheimer’s disease progression.

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References

65

[1]

The diagnosis of mild cognitive impairment due to Alzheimer's disease: Recommendations from the National Institute on Aging‐Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease

Marilyn S. Albert, Steven T. DeKosky, Dennis Dickson et al.

Alzheimer's & Dementia 2011 10.1016/j.jalz.2011.03.008

[2]

Atri "The Alzheimer's disease clinical Spectrum: Diagnosis and management" Med Clin North Am (2019) 10.1016/j.mcna.2018.10.009

[3]

Neugroschl "Alzheimer’s disease: Diagnosis and treatment across the spectrum of disease severity" Mt Sinai J Med (2011) 10.1002/msj.20279

[4]

NIA‐AA Research Framework: Toward a biological definition of Alzheimer's disease

Clifford R. Jack, David A. Bennett, Kaj Blennow et al.

Alzheimer's & Dementia 2018 10.1016/j.jalz.2018.02.018

[5]

Sartucci "Dysfunction of the magnocellular stream in Alzheimer's disease evaluated by pattern electroretinograms and visual evoked potentials" Brain Res Bull (2010) 10.1016/j.brainresbull.2010.04.001

[6]

Rizzo "Visual attention impairments in Alzheimer's disease" Neurology (2000) 10.1212/wnl.54.10.1954

[7]

Rizzo "Vision and cognition in Alzheimer's disease" Neuropsychologia (2000) 10.1016/s0028-3932(00)00023-3

[8]

Krasodomska "Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease" Doc Ophthalmol (2010) 10.1007/s10633-010-9238-x

[9]

Parisi "Morphological and functional retinal impairment in Alzheimer's disease patients" Clin Neurophysiol (2001) 10.1016/s1388-2457(01)00620-4

[10]

Gu "Exploring potential electrophysiological biomarkers in mild cognitive impairment: A systematic review and meta-analysis of event-related potential studies" J Alzheimers Dis (2017) 10.3233/jad-161286

[11]

Stothart "Early visual evoked potentials and mismatch negativity in Alzheimer's disease and mild cognitive impairment" J Alzheimers Dis (2015) 10.3233/jad-140930

[12]

Jacob "[Dysfunction of the magnocellular pathway in Alzheimer's disease]" Rev Neurol (Paris) (2002)

[13]

Hedges "P300 amplitude in Alzheimer's disease: A meta-analysis and meta-regression" Clin EEG Neurosci (2016) 10.1177/1550059414550567

[14]

Wiesman "Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer’s disease spectrum" Alzheimers Res Ther (2021) 10.1186/s13195-021-00881-w

[15]

Yener "A comparative analysis of sensory visual evoked oscillations with visual cognitive event related oscillations in Alzheimer's disease" Neurosci Lett (2009) 10.1016/j.neulet.2009.07.036

[16]

Iaccarino "Gamma frequency entrainment attenuates amyloid load and modifies microglia" Nature (2016) 10.1038/nature20587

[17]

Adaikkan "Gamma entrainment binds higher-order brain regions and offers neuroprotection" Neuron (2019) 10.1016/j.neuron.2019.04.011

[18]

Martorell "Multi-sensory gamma stimulation ameliorates Alzheimer’s-associated pathology and improves cognition" Cell (2019) 10.1016/j.cell.2019.02.014

[19]

Fiala "Ineffective phagocytosis of amyloid-beta by macrophages of Alzheimer's disease patients" J Alzheimers Dis (2005) 10.3233/jad-2005-7304

[20]

Vialatte "Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives" Prog Neurobiol (2010) 10.1016/j.pneurobio.2009.11.005

[21]

Angelini "Steady-state visual evoked potentials and phase synchronization in migraine patients" Phys Rev Lett (2004) 10.1103/physrevlett.93.038103

[22]

Shibata "Abnormal visual processing in migraine with aura: A study of steady-state visual evoked potentials" J Neurol Sci (2008) 10.1016/j.jns.2008.04.004

[23]

Clementz "Aberrant brain dynamics in schizophrenia: Delayed buildup and prolonged decay of the visual steady-state response" Brain Res Cogn Brain Res (2004) 10.1016/j.cogbrainres.2003.09.007

[24]

Jin "EEG Resonant responses in schizophrenia: A photic driving study with improved harmonic resolution" Schizophr Res (2000) 10.1016/s0920-9964(99)00211-x

[25]

Wilson "Cortical gamma generators suggest abnormal auditory circuitry in early-onset psychosis" Cereb Cortex (2008) 10.1093/cercor/bhm062

[26]

Wilson "Children and adolescents with autism exhibit reduced MEG steady-state gamma responses" Biol Psychiatry (2007) 10.1016/j.biopsych.2006.07.002

[27]

Herrmann "Human EEG responses to 1-100 hz flicker: Resonance phenomena in visual cortex and their potential correlation to cognitive phenomena" Exp Brain Res (2001) 10.1007/s002210100682

[28]

Pastor "Human cerebral activation during steady-state visual-evoked responses" J Neurosci (2003) 10.1523/jneurosci.23-37-11621.2003

[29]

The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on Aging‐Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease

Guy M. McKhann, David S. Knopman, Howard Chertkow et al.

Alzheimer's & Dementia 2011 10.1016/j.jalz.2011.03.005

[30]

Wechsler (2009)

[31]

Brandt (2001)

[32]

Wechsler (2008)

[33]

Heaton (2004)

[34]

Wechsler (2009)

[35]

The Montreal Cognitive Assessment, MoCA: A Brief Screening Tool For Mild Cognitive Impairment

Ziad S. Nasreddine, Natalie A. Phillips, Valérie Bédirian et al.

Journal of the American Geriatrics Society 2005 10.1111/j.1532-5415.2005.53221.x

[36]

“Mini-mental state”

Marshal F. Folstein, Susan E. Folstein, Paul R. McHugh

Journal of Psychiatric Research 1975 10.1016/0022-3956(75)90026-6

[37]

Pfeffer "Measurement of functional activities in older adults in the community" J Gerontol (1982) 10.1093/geronj/37.3.323

[38]

Minoshima "SNMMI Procedure standard/EANM practice guideline for amyloid PET imaging of the brain 1.0" J Nucl Med (2016) 10.2967/jnumed.116.174615

[39]

Performance Characteristics of Amyloid PET with Florbetapir F 18 in Patients with Alzheimer's Disease and Cognitively Normal Subjects

Abhinay D. Joshi, Michael J. Pontecorvo, Chrisopher M. Clark et al.

Journal of Nuclear Medicine 2012 10.2967/jnumed.111.090340

[40]

Taulu "Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements" Phys Med Biol (2006) 10.1088/0031-9155/51/7/008

[41]

Taulu "Suppression of interference and artifacts by the signal space separation method" Brain Topogr (2004) 10.1023/b:brat.0000032864.93890.f9

[42]

Uusitalo "Signal-space projection method for separating MEG or EEG into components" Med Biol Eng Comput (1997) 10.1007/bf02534144

[43]

Kovach "The demodulated band transform" J Neurosci Methods (2016) 10.1016/j.jneumeth.2015.12.004

[44]

Hoechstetter "BESA Source coherence: A new method to study cortical oscillatory coupling" Brain Topogr (2004) 10.1023/b:brat.0000032857.55223.5d

[45]

Papp "Critical evaluation of complex demodulation techniques for the quantification of bioelectrical activity" Biomed Sci Instrum (1977)

[46]

Spooner "Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention" Hum Brain Map (2020) 10.1002/hbm.24819

[47]

Wiesman "Aberrant occipital dynamics differentiate HIV-infected patients with and without cognitive impairment" Brain (2018) 10.1093/brain/awy097

[48]

Proskovec "Oscillatory dynamics in the dorsal and ventral attention networks during the reorienting of attention" Hum Brain Mapp (2018) 10.1002/hbm.23997

[49]

Gross "Dynamic imaging of coherent sources: Studying neural interactions in the human brain" Proc Natl Acad Sci U S A (2001) 10.1073/pnas.98.2.694

[50]

Hillebrand "A new approach to neuroimaging with magnetoencephalography" Hum Brain Mapp (2005) 10.1002/hbm.20102

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Details

Published: Jul 04, 2022
Vol/Issue: 4(4)
License: View

Authors

S

Seth D Springer

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA; College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA

A

Alex I Wiesman

College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA; Montreal Neurological Institute, McGill University , Montreal, QC H3A 2B4 , Canada

P

Pamela E May

College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA

M

Mikki Schantell

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA; College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA

H

Hallie J Johnson

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA

M

Madelyn P Willett

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA

C

Camilo A Castelblanco

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA

J

Jacob A Eastman

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA

N

Nicholas J Christopher-Hayes

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA; Center for Mind and Brain, University of California Davis , Davis, CA 95616 , USA

S

Sara L Wolfson

College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA

C

Craig M Johnson

College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA

D

Daniel L Murman

College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA; Memory Disorders & Behavioral Neurology Program, University of Nebraska Medical Center , Omaha, NE 68010 , USA

T

Tony W Wilson

Institute for Human Neuroscience, Boys Town National Research Hospital , Omaha, NE 68010 , USA; College of Medicine, University of Nebraska Medical Center , Omaha, NE 68198 , USA; Department of Pharmacology & Neuroscience, Creighton University , Omaha, NE 68178 , USA

Funding

National Institutes of Health Award: R01-MH116782 (TWW), R01-MH118013 (TWW), P20-GM144641 (TWW), RF1-MH117032 (TWW), F31-AG055332 (AIW), F32-NS119375

Cite This Article

Seth D Springer, Alex I Wiesman, Pamela E May, et al. (2022). Altered visual entrainment in patients with Alzheimer’s disease: magnetoencephalography evidence. Brain Communications, 4(4). https://doi.org/10.1093/braincomms/fcac198

Altered visual entrainment in patients with Alzheimer’s disease: magnetoencephalography evidence

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