Amnestic mild cognitive impairment (aMCI) is regarded as a transitional state of Alzheimer’s disease, with working memory (WM) impairment.
Objective:
To investigate the brain activity in aMCI patients during WM tasks with the functional near-infrared spectroscopy (fNIRS) technique, as well as explore the association between brain activity and cognitive function in multiple domains.
Methods:
This study is a case-control study of 54 aMCI patients and 33 cognitively healthy elderly (NC). All participants underwent neuropsychological assessments. fNIRS was applied to examine the brain activation during the WM task. Multivariable linear regression analysis was applied to evaluate associations between brain activation and cognitive function in multiple domains.
Results:
Compared to NC subjects, aMCI patients had lower activation in the bilateral prefrontal, parietal, and occipital cortex during the WM task. Additionally, activation in the left prefrontal, bilateral parietal, and occipital cortex during the encoding and maintenance phase was positively associated with memory function. During memory retrieval, higher activity in the left prefrontal, parietal, and occipital cortex were correlated with higher memory scores. Besides, a positive association also formed between attention function and the activation in the left prefrontal, parietal, and occipital cortex during the WM task.
Conclusion:
These findings demonstrated that reduced activation in the prefrontal, parietal and occipital cortex during WM might reflect the risk of cognitive impairment, especially memory and attention function in aMCI patients. Given the brain activation visualization, fNIRS may be a convenient and alternative tool for screening the risk of Alzheimer’s disease.
PetersenRC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med256, 183–194.
3.
LiJQ, TanL, WangHF, TanMS, TanL, XuW, ZhaoQF, WangJ, JiangT, YuJT (2016) Risk factors for predicting progression from mild cognitive impairment to Alzheimer’s disease: A systematic review and meta-analysis of cohort studies. J Neurol Neurosurg Psychiatry87, 476–484.
4.
MillerEK, LundqvistM, BastosAM (2018) Working Memory 2.0. Neuron100, 463–475.
5.
D’EspositoM, PostleBR (2015) The cognitive neuroscience of working memory. Annu Rev Psychol66, 115–142.
6.
GermanoC, KinsellaGJ (2005) Working memory and learning in early Alzheimer’s disease. Neuropsychol Rev15, 1–10.
7.
MandziaJL, McAndrewsMP, GradyCL, GrahamSJ, BlackSE (2009) Neural correlates of incidental memory in mild cognitive impairment: An fMRI study. Neurobiol Aging30, 717–730.
8.
SaykinAJ, WishartHA, RabinLA, FlashmanLA, McHughTL, MamourianAC, SantulliRB (2004) Cholinergic enhancement of frontal lobe activity in mild cognitive impairment. Brain127, 1574–1583.
9.
LouW, ShiL, WangD, TamCW, ChuWC, MokVC, ChengST, LamLC (2015) Decreased activity with increased background network efficiency in amnestic MCI during a visuospatial working memory task. Hum Brain Mapp36, 3387–3403.
10.
GoodmanMS, KumarS, ZomorrodiR, GhazalaZ, CheamA, BarrMS, DaskalakisZJ, BlumbergerDM, FischerC, FlintA, MahL, HerrmannN, BowieCR, MulsantBH, RajjiTK (2018) Theta-gamma coupling and working memory in Alzheimer’s dementia and mild cognitive impairment. Front Aging Neurosci10, 101.
11.
CicalesePA, LiR, AhmadiMB, WangC, FrancisJT, SelvarajS, SchulzPE, ZhangY (2020) An EEG-fNIRS hybridization technique in the four-class classification of Alzheimer’s disease. J Neurosci Methods336, 108618.
12.
BoasDA, ElwellCE, FerrariM, TagaG (2014) Twenty years of functional near-infrared spectroscopy: Introduction for the special issue. Neuroimage85 Pt 1, 1–5.
13.
NiuHJ, LiX, ChenYJ, MaC, ZhangJY, ZhangZJ (2013) Reduced frontal activation during a working memory task in mild cognitive impairment: A non-invasive near-infrared spectroscopy study. CNS Neurosci Ther19, 125–131.
14.
AraiH, TakanoM, MiyakawaK, OtaT, TakahashiT, AsakaH, KawaguchiT (2006) A quantitative near-infrared spectroscopy study: A decrease in cerebral hemoglobin oxygenation in Alzheimer’s disease and mild cognitive impairment. Brain Cogn61, 189–194.
15.
YangD, HongKS, YooSH, KimCS (2019) Evaluation of neural degeneration biomarkers in the prefrontal cortex for early identification of patients with mild cognitive impairment: An fNIRS study. Front Hum Neurosci13, 317.
16.
UemuraK, ShimadaH, DoiT, MakizakoH, TsutsumimotoK, ParkH, SuzukiT, (2016) Reduced prefrontal oxygenation in mild cognitive impairment during memory retrieval. Int J Geriatr Psychiatry31, 583–591.
17.
YuJW, LimSH, KimB, KimE, KimK, KyuPS, SeokBY, SakongJ, ChoiJW (2020) Prefrontal functional connectivity analysis of cognitive decline for early diagnosis of mild cognitive impairment: A functional near-infrared spectroscopy study. Biomed Opt Express11, 1725–1741.
18.
HahnB, RobinsonBM, LeonardCJ, LuckSJ, GoldJM (2018) Posterior parietal cortex dysfunction is central to working memory storage and broad cognitive deficits in schizophrenia. J Neurosci38, 8378–8387.
YuQ, ShimWM (2017) Occipital, parietal, and frontal cortices selectively maintain task-relevant features of multi-feature objects in visual working memory. Neuroimage157, 97–107.
21.
BomyeaJ, TaylorCT, SpadoniAD, SimmonsAN (2018) Neural mechanisms of interference control in working memory capacity. Hum Brain Mapp39, 772–782.
22.
LuJ, LiD, LiF, ZhouA, WangF, ZuoX, JiaXF, SongH, JiaJ (2011) Montreal cognitive assessment in detecting cognitive impairment in Chinese elderly individuals: A population-based study. J Geriatr Psychiatry Neurol24, 184–190.
23.
LiQ, FengJ, GuoJ, WangZ, LiP, LiuH, FanZ (2020) Effects of the multisensory rehabilitation product for home-based hand training after stroke on cortical activation by using NIRS methods. Neurosci Lett717, 134682.
24.
SutokoS, MondenY, TokudaT, IkedaT, NagashimaM, FunaneT, AtsumoriH, KiguchiM, MakiA, YamagataT, DanI (2020) Atypical dynamic-connectivity recruitment in attention-deficit/hyperactivity disorder children: An insight into task-based dynamic connectivity through an fNIRS study. Front Hum Neurosci14, 3.
25.
HomaeF, WatanabeH, OtobeT, NakanoT, GoT, KonishiY, TagaG (2010) Development of global cortical networks in early infancy. J Neurosci30, 4877–4882.
26.
HoshiY (2003) Functional near-infrared optical imaging: Utility and limitations in human brain mapping. Psychophysiology40, 511–520.
27.
KimH (2019) Neural activity during working memory encoding, maintenance, and retrieval: A network-based model and meta-analysis. Hum Brain Mapp40, 4912–4933.
28.
LeavittML, PieperF, SachsAJ, Martinez-TrujilloJC (2017) Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles. Proc Natl Acad Sci U S A114, E2494–E2503.
29.
CurtisCE, SpragueTC (2021) Persistent activity during working memory from front to back. Front Neural Circuits15, 696060.
30.
RawleyJB, ConstantinidisC (2009) Neural correlates of learning and working memory in the primate posterior parietal cortex. Neurobiol Learn Mem91, 129–138.
31.
van KerkoerleT, SelfMW, RoelfsemaPR (2017) Layer-specificity in the effects of attention and working memory on activity in primary visual cortex. Nat Commun8, 13804.
32.
BettencourtKC, XuY (2016) Decoding the content of visual short-term memory under distraction in occipital and parietal areas. Nat Neurosci19, 150–157.
33.
LeeSH, KravitzDJ, BakerCI (2013) Goal-dependent dissociation of visual and prefrontal cortices during working memory. Nat Neurosci16, 997–999.
34.
SpragueTC, SerencesJT (2013) Attention modulates spatial priority maps in the human occipital, parietal and frontal cortices. Nat Neurosci16, 1879–1887.
35.
BokdeAL, KarmannM, BornC, TeipelSJ, OmerovicM, EwersM, FrodlT, MeisenzahlE, ReiserM, MollerHJ, HampelH (2010) Altered brain activation during a verbal working memory task in subjects with amnestic mild cognitive impairment. J Alzheimers Dis21, 103–118.
36.
BadgaiyanRD, SchacterDL, AlpertNM (2002) Retrieval of relational information: A role for the left inferior prefrontal cortex. Neuroimage17, 393–400.
37.
SupeèrH, SpekreijseH, LammeVAF (2001) A neural correlate of working memory in the monkey primary visual cortex. Science293, 120–124.
38.
CheinJM, MooreAB, ConwayAR (2011) Domain-general mechanisms of complex working memory span. Neuroimage54, 550–559.
39.
XieS, XiaoJ, BaiJ, JiangX (2004) Memory tasks in normal aged volunteers: An fMRI study. Chin J Med Imaging Technol20, 571–574.
40.
BerryhillME, CheinJ, OlsonIR (2011) At the intersection of attention and memory: The mechanistic role of the posterior parietal lobe in working memory. Neuropsychologia49, 1306–1315.
41.
TakaseR, BoasenJ, KurikiS, ToyomuraA, YokosawaK (2022) Processing time affects sequential memory performance beginning at the level of visual encoding. PLoS One17, e0265719.
42.
XieY, LiY, DuanH, XuX, ZhangW, FangP (2021) Theta oscillations and source connectivity during complex audiovisual object encoding in working memory. Front Hum Neurosci15, 614950.
43.
MachuldaMM, SenjemML, WeigandSD, SmithGE, IvnikRJ, BoeveBF, KnopmanDS, PetersenRC, JackCR (2009) Functional magnetic resonance imaging changes in amnestic and nonamnestic mild cognitive impairment during encoding and recognition tasks. J Int Neuropsychol Soc15, 372–382.
44.
PasquierF, GrymonprezL, LebertF, Van der LindenM (2001) Memory impairment differs in frontotemporal dementia and Alzheimer’s disease. Neurocase7, 161–171.
45.
KarraschM, LaineM, RinneJO, RapinojaP, SinervaE, KrauseCM (2006) Brain oscillatory responses to an auditory-verbal working memory task in mild cognitive impairment and Alzheimer’s disease. Int J Psychophysiol59, 168–178.
46.
KochanNA, BreakspearM, SlavinMJ, ValenzuelaM, McCrawS, BrodatyH, SachdevPS (2010) Functional alterations in brain activation and deactivation in mild cognitive impairment in response to a graded working memory challenge. Dement Geriatr Cogn Disord30, 553–568.
47.
RosenWG (1983) Clinical and neuropsychological assessment of Alzheimer disease. Adv Neurol38, 51–64.
48.
RomoR, BrodyCD, HernandezA, LemusL (1999) Neuronal correlates of parametric working memory in the prefrontal cortex. Nature399, 470–473.
49.
FunahashiS, BruceCJ, Goldman-RakicPS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol61, 331–349.
50.
InagakiHK, FontolanL, RomaniS, SvobodaK (2019) Discrete attractor dynamics underlies persistent activity in the frontal cortex. Nature566, 212–217.
51.
CuiL, ZhangZ, ZacLC, GuoQ (2021) Local functional MR change pattern and its association with cognitive function in objectively-defined subtle cognitive decline. Front Aging Neurosci13, 684918.
52.
NiL, ZhaoM, HuZ, YangK, ZhaoX, NiuH, LinH (2021) Neural mechanism of Shentai tea polyphenols on cognitive improvements for individuals with subjective cognitive decline: A functional near-infrared spectroscopy study. J Alzheimers Dis82, 1137–1145.
53.
RickerTJ, NieuwensteinMR, BaylissDM, BarrouilletP (2018) Working memory consolidation: Insights from studies on attention and working memory. Ann N Y Acad Sci1424, 8–18.
54.
EsterEF, SuttererDW, SerencesJT, AwhE (2016) Feature-selective attentional modulations in human frontoparietal cortex. J Neurosci36, 8188–8199.
55.
LiuT, HospadarukL, ZhuDC, GardnerJL (2011) Feature-specific attentional priority signals in human cortex. J Neurosci31, 4484–4495.
56.
JeheeJF, BradyDK, TongF (2011) Attention improves encoding of task-relevant features in the human visual cortex. J Neurosci31, 8210–8219.
57.
KastnerS, DeSimoneK, KonenCS, SzczepanskiSM, WeinerKS, SchneiderKA (2007) Topographic maps in human frontal cortex revealed in memory-guided saccade and spatial working-memory tasks. J Neurophysiol97, 3494–3507.
58.
SilverMA, RessD, HeegerDJ (2005) Topographic maps of visual spatial attention in human parietal cortex. J Neurophysiol94, 1358–1371.
59.
SilvaP, SpedoCT, BarreiraAA, LeoniRF (2018) Symbol digit modalities test adaptation for magnetic resonance imaging environment: A systematic review and meta-analysis. Mult Scler Relat Disord20, 136–143.
60.
JenesonA, SquireLR (2012) Working memory, long-term memory, and medial temporal lobe function. Learn Mem19, 15–25.
61.
RanganathC (2006) Working memory for visual objects: Complementary roles of inferior temporal, medial temporal, and prefrontal cortex. {Neuroscience139, 277–289.
