Event-related potentials (ERPs) are valuable tools for the early detection and monitoring of cognitive impairment in people with Multiple Sclerosis (pwMS) and towards the evaluation of the effectiveness of treatment. The Symbol Digit Modalities Test (SDMT), a screening tool for cognitive dysfunction, is often impaired in pwMS.
Objective:
To explore the ERPs and reaction time (RT) correlates of SDMT as indicators of cognitive impairment in pwMS.
Methods:
We developed an EEG-compatible (EEG-SDMT) paradigm. Ninety-two pwMS and twenty-eight healthy controls (HC) underwent ERPs and RT measurement during EEG-SDMT.
Results:
SDMT-ERPs presented a centro-parietal (Pz electrode) positive peak (P5) with a significantly longer latency in pwMS (611.72 ± 122.30 ms) versus HC (517.29 ± 75.53 ms) (p < 0.01). RTs and raw scores in the standard SDMT were inversely correlated (r = −.722, p < .001).
Conclusion:
Our EEG-SDMT paradigm identified neurophysiological correlates of SDMT performance, which was significantly affected in pwMS. Although the P5 showed longer latencies in pwMS, this component did not differentiate between cognitively impaired and preserved individuals, likely because it is still too early to capture higher-order cognitive deficits. In contrast, RTs emerged as a more reliable and sensitive indicator of cognitive performance.
ChiaravallotiNDDeLucaJ.Cognitive impairment in multiple sclerosis. Lancet Neurol2008; 7(12): 1139–1151.
2.
AmatoMPMorraVBFalautanoM, et al. Cognitive assessment in multiple sclerosis – An Italian consensus. Neurol Sci2018; 39: 1317–1324.
3.
AmatoMPZipoliVPortaccioE.Cognitive changes in multiple sclerosis. Expert Rev Neurother2008; 8(10): 1585–1596.
4.
MitchellAJBenito-LeónJGonzálezJM, et al. Quality of life and its assessment in multiple sclerosis: Integrating physical and psychological components of wellbeing. Lancet Neurol2005; 4(9): 556–566.
5.
SmithA.Symbol digit modalities test (The Clinical Neuropsychologist). Los Angeles, CA: Western Psychological Services, 1973.
6.
SandryJSimonetDVBrandstadterR, et al. The Symbol Digit Modalities Test (SDMT) is sensitive but non-specific in MS: Lexical access speed, memory, and information processing speed independently contribute to SDMT performance. Mult Scler Relat Disord2021; 51: 102950.
7.
KalbRBeierMBenedictRH, et al. Recommendations for cognitive screening and management in multiple sclerosis care. Mult Scler2018; 24(13): 1665–1680.
8.
AkbarNHonarmandKKouN, et al. Validity of a computerized version of the symbol digit modalities test in multiple sclerosis. J Neurol2011; 258(3): 373–379.
9.
ChenXHuNGaoX.Development of a brain-computer interface–based symbol digit modalities test and validation in healthy elderly volunteers and stroke patients. IEEE Trans Neural Syst Rehabil Eng2022; 30: 1433–1440.
10.
van OirschotPHeeringsMWendrichK, et al. Symbol digit modalities test variant in a smartphone app for persons with multiple sclerosis: Validation study. JMIR Mhealth Uhealth2020; 8(10): e18160.
11.
SundgrenMNikulinVVMaurexL, et al. P300 amplitude and response speed relate to preserved cognitive function in relapsing–remitting multiple sclerosis. Clin Neurophysiol2015; 126(4): 689–697.
12.
ChinnaduraiSAVenkatesanSAShankarG, et al. A study of cognitive fatigue in multiple sclerosis with novel clinical and electrophysiological parameters utilizing the event related potential P300. Mult Scler Relat Disord2016; 10: 1–6.
13.
ZweckerMSarovaILavieM, et al. Detection of cognitive impairment in multiple sclerosis based on P300 event-related potential. Int J Phys Med Rehabil2018; 6(4): 479.
14.
MagnanoIAielloIPirasMR.Cognitive impairment and neurophysiological correlates in MS. J Neurol Sci2006; 245(1–2): 117–122.
15.
PolichJHerbstKL.P300 as a clinical assay: Rationale, evaluation, and findings. Int J Psychophysiol2000; 38(1): 3–19.
16.
PirasMRMagnanoICanuED, et al. Longitudinal study of cognitive dysfunction in multiple sclerosis: Neuropsychological, neuroradiological, and neurophysiological findings. J Neurol Neurosurg Psychiatry2003; 74(7): 878–885.
17.
LeocaniLGonzalez-RosaJJComiG.Neurophysiological correlates of cognitive disturbances in multiple sclerosis. Neurol Sci2010; 31(Suppl. 2): S249–53.
18.
BenedictRHAmatoMPBoringaJ, et al. Brief International Cognitive Assessment for MS (BICAMS): International standards for validation. BMC Neurol2012; 12: 1–7.
19.
ThompsonAJBanwellBLBarkhofF, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol2018; 17(2): 162–173.
20.
DelisDC.California Verbal Learning Test. San Antonio, TX: Psychological Corporation, 2000.
21.
BenedictRHSchretlenDGroningerL, et al. Revision of the brief visuospatial memory test: Studies of normal performance, reliability, and validity. Psychol Assess1996; 8(2): 145.
22.
GorettiBNiccolaiCHakikiB, et al. The Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS): Normative values with gender, age and education corrections in the Italian population. BMC Neurol2014; 14: 1–6.
23.
GrattonGColesMGDonchinE.A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol1983; 55(4): 468–484.
24.
PictonTW.The P300 wave of the human event-related potential. J Clin Neurophysiol1992; 9(4): 456–479.
25.
MartínezADi RussoFAnllo-VentoL, et al. Putting spatial attention on the map: Timing and localization of stimulus selection processes in striate and extrastriate visual areas. Vision Res2001; 41(10-11): 1437–1457.
26.
FargierRBürkiAPinetS, et al. Word onset phonetic properties and motor artifacts in speech production EEG recordings. Psychophysiology2018; 55(2): 12982.
27.
PolichJMargalaC.P300 and probability: Comparison of oddball and single-stimulus paradigms. Int J Psychophysiol1997; 25(2): 169–176.
28.
CoveyTJShucardJLShucardDW.Event-related brain potential indices of cognitive function and brain resource reallocation during working memory in patients with multiple sclerosis. Clin Neurophysiol2017; 128(4): 604–621.
29.
SpeerMESoldanA.Cognitive reserve modulates ERPs associated with verbal working memory in healthy younger and older adults. Neurobiol Aging2015; 36(3): 1424–1434.
30.
ImaniEHaratiAPourrezaH, et al. Brain–behavior relationships in the perceptual decision-making process through cognitive processing stages. Neuropsychologia2021; 155: 107821.
31.
DanaARafieeSGholamiA.Motor reaction time and accuracy in patients with multiple sclerosis: Effects of an active computerized training program. Neurol Sci2019; 40(9): 1849–1854.
32.
ReickerLITombaughTNWalkerL, et al. Reaction time: An alternative method for assessing the effects of multiple sclerosis on information processing speed. Arch Clin Neuropsychol2007; 22(5): 655–664.
33.
HsuWYRowlesWAngueraJA, et al. Assessing cognitive function in multiple sclerosis with digital tools: Observational study. J Med Internet Res2021; 23(12): e25748.
