Visuospatial alpha and gamma oscillations scale with the severity of cognitive dysfunction in patients on the Alzheimer's disease spectrum.
Alzheimer’s disease
Magnetoencephalography
Neural oscillations
Source imaging
Visuospatial processing
Journal
Alzheimer's research & therapy
ISSN: 1758-9193
Titre abrégé: Alzheimers Res Ther
Pays: England
ID NLM: 101511643
Informations de publication
Date de publication:
17 08 2021
17 08 2021
Historique:
received:
26
01
2021
accepted:
28
07
2021
entrez:
18
8
2021
pubmed:
19
8
2021
medline:
14
9
2021
Statut:
epublish
Résumé
Entrainment of neural oscillations in occipital cortices by external rhythmic visual stimuli has been proposed as a novel therapy for patients with Alzheimer's disease (AD). Despite this increased interest in visual neural oscillations in AD, little is known regarding their role in AD-related cognitive impairment and in particular during visuospatial processing. We used source-imaged magnetoencephalography (MEG) and an established visuospatial processing task to elicit multi-spectral neuronal responses in 35 biomarker-confirmed patients on the AD spectrum and 20 biomarker-negative older adults. Neuronal oscillatory responses were imaged to the level of the cortex, and group classifications and neurocognitive relationships were modeled using logistic and linear regression, respectively. Visuospatial neuronal oscillations in the theta, alpha, and gamma ranges significantly predicted the classification of patients on the AD spectrum. Importantly, the direction of these effects differed by response frequency, such that patients on the AD spectrum exhibited weaker alpha-frequency responses in lateral occipital regions, and stronger gamma-frequency responses in the primary visual cortex, as compared to biomarker-negative older adults. In addition, alpha and gamma, but not theta, oscillations robustly predicted cognitive status (i.e., MoCA and MMSE scores), such that patients with neural responses that deviated more from those of healthy older adults exhibited poorer cognitive performance. We find that the multi-spectral neural dynamics supporting visuospatial processing differentiate patients on the AD spectrum from cognitively normal, biomarker-negative older adults. Oscillations in the alpha and gamma bands also relate to cognitive status in ways that are informative for emerging clinical interventions.
Sections du résumé
BACKGROUND
Entrainment of neural oscillations in occipital cortices by external rhythmic visual stimuli has been proposed as a novel therapy for patients with Alzheimer's disease (AD). Despite this increased interest in visual neural oscillations in AD, little is known regarding their role in AD-related cognitive impairment and in particular during visuospatial processing.
METHODS
We used source-imaged magnetoencephalography (MEG) and an established visuospatial processing task to elicit multi-spectral neuronal responses in 35 biomarker-confirmed patients on the AD spectrum and 20 biomarker-negative older adults. Neuronal oscillatory responses were imaged to the level of the cortex, and group classifications and neurocognitive relationships were modeled using logistic and linear regression, respectively.
RESULTS
Visuospatial neuronal oscillations in the theta, alpha, and gamma ranges significantly predicted the classification of patients on the AD spectrum. Importantly, the direction of these effects differed by response frequency, such that patients on the AD spectrum exhibited weaker alpha-frequency responses in lateral occipital regions, and stronger gamma-frequency responses in the primary visual cortex, as compared to biomarker-negative older adults. In addition, alpha and gamma, but not theta, oscillations robustly predicted cognitive status (i.e., MoCA and MMSE scores), such that patients with neural responses that deviated more from those of healthy older adults exhibited poorer cognitive performance.
CONCLUSIONS
We find that the multi-spectral neural dynamics supporting visuospatial processing differentiate patients on the AD spectrum from cognitively normal, biomarker-negative older adults. Oscillations in the alpha and gamma bands also relate to cognitive status in ways that are informative for emerging clinical interventions.
Identifiants
pubmed: 34404472
doi: 10.1186/s13195-021-00881-w
pii: 10.1186/s13195-021-00881-w
pmc: PMC8369319
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
139Subventions
Organisme : NIA NIH HHS
ID : F31 AG055332
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA047828
Pays : United States
Organisme : NINDS NIH HHS
ID : F32 NS119375
Pays : United States
Organisme : NIMH NIH HHS
ID : RF1 MH117032
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH118013
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH116782
Pays : United States
Informations de copyright
© 2021. The Author(s).
Références
Neuroimage. 2019 Jan 15;185:513-520
pubmed: 30321644
J Gerontol. 1982 May;37(3):323-9
pubmed: 7069156
J Neurosci Methods. 2007 Apr 15;161(2):342-50
pubmed: 17156848
J Neural Transm (Vienna). 2008 Sep;115(9):1301-11
pubmed: 18607528
Neuroimage. 2002 Nov;17(3):1403-14
pubmed: 12414280
Clin Neurophysiol. 2017 Aug;128(8):1426-1437
pubmed: 28622527
Curr Alzheimer Res. 2019;16(1):67-89
pubmed: 30345915
Sci Transl Med. 2020 Mar 11;12(534):
pubmed: 32161102
Curr Opin Neurol. 2013 Dec;26(6):662-70
pubmed: 24150222
Science. 2002 Jan 25;295(5555):690-4
pubmed: 11809976
J Psychiatr Res. 1975 Nov;12(3):189-98
pubmed: 1202204
Nature. 2016 Dec 7;540(7632):230-235
pubmed: 27929004
J Nucl Med. 2012 Mar;53(3):378-84
pubmed: 22331215
Phys Med Biol. 2006 Apr 7;51(7):1759-68
pubmed: 16552102
Brain. 2018 Jun 1;141(6):1678-1690
pubmed: 29672678
J Alzheimers Dis. 2012;31 Suppl 3:S117-35
pubmed: 22810101
Cereb Cortex. 2021 Jun 10;31(7):3353-3362
pubmed: 33611348
Int J Psychophysiol. 2020 Sep;155:41-48
pubmed: 32522511
J Alzheimers Dis. 2013;37(4):759-67
pubmed: 23948923
Cortex. 2018 Nov;108:222-233
pubmed: 30261367
Neurol Neuroimmunol Neuroinflamm. 2020 Feb 26;7(3):
pubmed: 32102916
Med Biol Eng Comput. 1997 Mar;35(2):135-40
pubmed: 9136207
Alzheimers Dement (Amst). 2021 May 31;13(1):e12200
pubmed: 34095434
Alzheimers Res Ther. 2021 Feb 5;13(1):35
pubmed: 33546722
J Cogn Neurosci. 2011 Sep;23(9):2494-502
pubmed: 20681750
Alzheimers Dement. 2017 Apr;13(4):e1-e85
pubmed: 28342697
Int J Psychophysiol. 2000 Dec 1;38(3):211-23
pubmed: 11102663
Behav Brain Res. 2021 Jan 1;396:112904
pubmed: 32941881
Neuroimage. 2005 Oct 1;27(4):835-41
pubmed: 15961323
Front Hum Neurosci. 2010 Nov 04;4:186
pubmed: 21119777
Neuroimage. 2013 Apr 1;69:223-30
pubmed: 23274186
Front Psychol. 2014 Feb 07;5:74
pubmed: 24570669
Neurosci Lett. 2009 Oct 25;462(3):193-7
pubmed: 19616074
Front Comput Neurosci. 2018 Aug 23;12:60
pubmed: 30190674
Neuron. 2019 Jun 5;102(5):929-943.e8
pubmed: 31076275
J Neurosci. 2000 Mar 15;20(6):RC63
pubmed: 10704517
Cereb Cortex. 2008 Feb;18(2):386-96
pubmed: 17556771
J Am Geriatr Soc. 2005 Apr;53(4):695-9
pubmed: 15817019
Pflugers Arch. 2018 Sep;470(9):1377-1389
pubmed: 29808353
Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):694-9
pubmed: 11209067
Psychiatry Res. 2007 Oct 15;156(1):43-57
pubmed: 17719211
Hum Brain Mapp. 2017 Oct;38(10):5128-5140
pubmed: 28714584
Alzheimers Dement (Amst). 2017 Nov 06;10:66-74
pubmed: 29780858
J Neurophysiol. 2011 Mar;105(3):1318-26
pubmed: 21228304
Cogn Neurodyn. 2010 Dec;4(4):263-74
pubmed: 22132038
Trends Neurosci. 2020 Jan;43(1):24-41
pubmed: 31836315
Int J Psychophysiol. 1992 Sep;13(2):147-60
pubmed: 1399754
Neuroimage. 2020 Nov 1;221:117192
pubmed: 32711061
J Nucl Med. 2016 Aug;57(8):1316-22
pubmed: 27481605
Alzheimers Dement. 2017 Mar;13(3):205-216
pubmed: 27697430
Cell. 2019 Apr 4;177(2):256-271.e22
pubmed: 30879788
J Neurosci Methods. 2016 Mar 1;261:135-54
pubmed: 26711370
Alzheimers Dement. 2011 May;7(3):263-9
pubmed: 21514250
J Neurophysiol. 2006 Jun;95(6):3844-51
pubmed: 16571739
Alzheimers Res Ther. 2017 Aug 9;9(1):60
pubmed: 28793924
Nat Neurosci. 2017 Feb 23;20(3):327-339
pubmed: 28230841
Neuroimage. 2006 Oct 15;33(1):127-38
pubmed: 16904911
Cereb Cortex. 2019 Jul 22;29(8):3505-3513
pubmed: 30215685
Int J Psychophysiol. 2001 Jan;39(2-3):241-8
pubmed: 11163901
Biomed Sci Instrum. 1977 Apr 25-27;13:135-45
pubmed: 871500
Nat Protoc. 2018 Aug;13(8):1850-1868
pubmed: 30072722