Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T12:01:38.101Z Has data issue: false hasContentIssue false
  • English
  • Français

The reduced left hippocampal volume related to the delayed P300 latency in amnestic mild cognitive impairment

Published online by Cambridge University Press:  20 April 2020

Lijuan Gao ,
Lihua Gu ,
Hao Shu ,
Jiu Chen ,
Jianli Zhu ,
Bi Wang ,
Yachen Shi ,
Ruize Song ,
Kun Li  and
Xianrui Li
...Show all authors
Lijuan Gao
Affiliation:
Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Institution of Neuropsychiatry, Southeast University, Nanjing, Jiangsu210009, China
Lihua Gu
Affiliation:
Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Institution of Neuropsychiatry, Southeast University, Nanjing, Jiangsu210009, China
Hao Shu
Affiliation:
Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Institution of Neuropsychiatry, Southeast University, Nanjing, Jiangsu210009, China
Jiu Chen
Affiliation:
Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Institution of Neuropsychiatry, Southeast University, Nanjing, Jiangsu210009, China
Jianli Zhu
Affiliation:
Department of Psychology, Xinxiang Medical University, Xinxiang, Henan453003, China
Bi Wang
Affiliation:
Department of Radiology, Henan Mental Hospital, the Second Affiliated Hospital of Xinxiang Medical University, Xinxiang, Henan453002, China
Yachen Shi
Affiliation:
Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Institution of Neuropsychiatry, Southeast University, Nanjing, Jiangsu210009, China
Ruize Song
Affiliation:
Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Institution of Neuropsychiatry, Southeast University, Nanjing, Jiangsu210009, China
Kun Li
Affiliation:
Department of Psychology, Xinxiang Medical University, Xinxiang, Henan453003, China
Xianrui Li
Affiliation:
Department of Psychology, Xinxiang Medical University, Xinxiang, Henan453003, China
Haisan Zhang
Affiliation:
Department of Radiology, Henan Mental Hospital, the Second Affiliated Hospital of Xinxiang Medical University, Xinxiang, Henan453002, China
Hongxing Zhang
Affiliation:
Department of Psychology, Xinxiang Medical University, Xinxiang, Henan453003, China
Zhijun Zhang*
Affiliation:
Department of Neurology, Affiliated ZhongDa Hospital, School of Medicine, Institution of Neuropsychiatry, Southeast University, Nanjing, Jiangsu210009, China Department of Psychology, Xinxiang Medical University, Xinxiang, Henan453003, China
*
Author for correspondence: Zhijun Zhang, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Amnestic mild cognitive impairment (aMCI) is characterized by delayed P300 latency and reduced grey matter (GM) volume, respectively. The relationship between the features in aMCI is unclear. This study was to investigate the relationship between the altered P300 latency and the GM volume in aMCI.

Methods

Thirty-four aMCI and 34 well-matched normal controls (NC) were studied using electroencephalogram during a visual oddball task and scanned with MRI. Both tests were finished in the same day.

Results

As compared with the NC group, the aMCI group exhibited delayed P300 latency in parietal cortex and reduced GM volumes in bilateral temporal pole and left hippocampus/parahippocampal gyrus. A remarkable negative correlation was found between delayed P300 latency and reduced left hippocampal volume only in the aMCI group. Interestingly, the mediating analysis found P300 latency significantly mediated the association between right supramarginal gyrus volume and information processing speed indicated by Stroop Color and Word Test A scores.

Conclusions

The association between delayed P300 latency and reduced left hippocampal volume in aMCI subjects suggests that reduced left hippocampal volume may be the potential structural basis of delayed P300 latency.

Keywords

Amnestic mild cognitive impairmentP300event-related potentialMRImediating effect
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 12 , September 2021 , pp. 2054 - 2062
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Babic Leko, M., Krbot Skoric, M., Klepac, N., Borovecki, F., Langer Horvat, L., Vogrinc, Z., & Simic, G. (2018). Event-related potentials improve the efficiency of cerebrospinal fluid biomarkers for differential diagnosis of Alzheimer's disease. Current Alzheimer Research, 15(13), 1244–1260. doi: 10.2174/1567205015666180911151116.CrossRefGoogle ScholarPubMed
Bledowski, C., Prvulovic, D., Goebel, R., Zanella, F. E., & Linden, D. E. (2004a). Attentional systems in target and distractor processing: A combined ERP and fMRI study. Neuroimage, 22(2), 530–540. doi: 10.1016/j.neuroimage.2003.12.034.CrossRefGoogle Scholar
Bledowski, C., Prvulovic, D., Hoechstetter, K., Scherg, M., Wibral, M., Goebel, R., & Linden, D. E. (2004b). Localizing P300 generators in visual target and distractor processing: A combined event-related potential and functional magnetic resonance imaging study. Journal of Neuroscience, 24(42), 9353–9360. doi: 10.1523/jneurosci.1897-04.2004.CrossRefGoogle Scholar
Bogerts, B. (1997). The temporolimbic system theory of positive schizophrenic symptoms. Schizophrenia Bulletin, 23(3), 423–435. doi: 10.1093/schbul/23.3.423.CrossRefGoogle ScholarPubMed
Bonanni, L., Franciotti, R., Onofrj, V., Anzellotti, F., Mancino, E., Monaco, D., … Onofrj, M. (2010). Revisiting P300 cognitive studies for dementia diagnosis: Early dementia with Lewy bodies (DLB) and Alzheimer disease (AD). Neurophysiologie Clinique, 40(5–6), 255–265. doi: 10.1016/j.neucli.2010.08.001.CrossRefGoogle Scholar
Bramon, E., McDonald, C., Croft, R. J., Landau, S., Filbey, F., Gruzelier, J. H., … Murray, R. M. (2005). Is the P300 wave an endophenotype for schizophrenia? A meta-analysis and a family study. Neuroimage, 27(4), 960–968. doi: 10.1016/j.neuroimage.2005.05.022.CrossRefGoogle Scholar
Chen, L., Zhou, Y., Liu, L., Zhang, X., Zhang, H., & Liu, S. (2015). Cortical event-related potentials in Alzheimer's disease and frontotemporal lobar degeneration. Journal of the Neurological Sciences, 359(1–2), 88–93. doi: 10.1016/j.jns.2015.10.040.CrossRefGoogle ScholarPubMed
Dutt, A., Ganguly, T., Shaikh, M., Walshe, M., Schulze, K., Marshall, N., … Bramon, E. (2012). Association between hippocampal volume and P300 event related potential in psychosis: Support for the Kraepelinian divide. Neuroimage, 59(2), 997–1003. doi: 10.1016/j.neuroimage.2011.08.067.CrossRefGoogle ScholarPubMed
Eckerström, C., Olsson, E., Borga, M., Ekholm, S., Ribbelin, S., Rolstad, S., … Malmgren, H. (2008). Small baseline volume of left hippocampus is associated with subsequent conversion of MCI into dementia: The Göteborg MCI study. Journal of the Neurological Sciences, 272(1–2), 48–59. doi: 10.1016/j.jns.2008.04.024.CrossRefGoogle ScholarPubMed
Fritz, H. C., Wittfeld, K., Schmidt, C. O., Domin, M., Grabe, H. J., Hegenscheid, K., … Lotze, M. (2014). Current smoking and reduced gray matter volume-a voxel-based morphometry study. Neuropsychopharmacology, 39(11), 2594–2600. doi: 10.1038/npp.2014.112.CrossRefGoogle ScholarPubMed
Fruehwirt, W., Dorffner, G., Roberts, S., Gerstgrasser, M., Grossegger, D., Schmidt, R., … Benke, T. (2019). Associations of event-related brain potentials and Alzheimer's disease severity: A longitudinal study. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 92, 31–38. doi: 10.1016/j.pnpbp.2018.12.013.CrossRefGoogle ScholarPubMed
Fusar-Poli, P., Crossley, N., Woolley, J., Carletti, F., Perez-Iglesias, R., Broome, M., … McGuire, P. (2011). Gray matter alterations related to P300 abnormalities in subjects at high risk for psychosis: Longitudinal MRI-EEG study. Neuroimage, 55(1), 320–328. doi: 10.1016/j.neuroimage.2010.11.075.CrossRefGoogle ScholarPubMed
Fushimi, M., Matsubuchi, N., & Sekine, A. (2005). Progression of P300 in a patient with bilateral hippocampal lesions. Clinical Neurophysiology, 116(3), 625–631.CrossRefGoogle Scholar
Geng, J. J., & Vossel, S. (2013). Re-evaluating the role of TPJ in attentional control: Contextual updating? Neuroscience and Biobehavioral Reviews, 37(10 Pt 2), 2608–2620. doi: 10.1016/j.neubiorev.2013.08.010CrossRefGoogle ScholarPubMed
Gong, L., Yin, Y., He, C., Ye, Q., Bai, F., Yuan, Y., … Zhang, Z. (2017). Disrupted reward circuits is associated with cognitive deficits and depression severity in major depressive disorder. Journal of Psychiatric Research, 84, 9–17.CrossRefGoogle ScholarPubMed
Gordon, E., Kraiuhin, C., Harris, A., Meares, R., & Howson, A. (1986). The differential diagnosis of dementia using P300 latency. Biological Psychiatry, 21(12), 1123–1132.CrossRefGoogle ScholarPubMed
Guo, Q., Tang, Y., Li, H., Zhang, T., Li, J., Sheng, J., … Wang, J. (2014). Both volumetry and functional connectivity of Heschl's gyrus are associated with auditory P300 in first episode schizophrenia. Schizophrenia Research, 160(1–3), 57–66. doi: 10.1016/j.schres.2014.10.006.CrossRefGoogle ScholarPubMed
Holt, L. E., Raine, A., Pa, G., Schneider, L. S., Henderson, V. W., & Pollock, V. E. (1995). P300 topography in Alzheimer's disease. Psychophysiology, 32(3), 257–265.CrossRefGoogle ScholarPubMed
Howe, A. S., Bani-Fatemi, A., & De Luca, V. (2014). The clinical utility of the auditory P300 latency subcomponent event-related potential in preclinical diagnosis of patients with mild cognitive impairment and Alzheimer's disease. Brain and Cognition, 86, 64–74. doi: 10.1016/j.bandc.2014.01.015.CrossRefGoogle ScholarPubMed
Jack, C. R., Bennett, D. A., Blennow, K., Carrillo, M. C., Dunn, B., Haeberlein, S. B., … Sperling, R. (2018). NIA-AA Research Framework: Toward a biological definition of Alzheimer's disease. Alzheimer's & Dementia: The Journal of the Alzheimer's Association, 14(4), 535–562. doi: 10.1016/j.jalz.2018.02.018.CrossRefGoogle Scholar
Jeon, Y. W., & Polich, J. (2003). Meta-analysis of P300 and schizophrenia: Patients, paradigms, and practical implications. Psychophysiology, 40(5), 684–701.CrossRefGoogle ScholarPubMed
Jiang, S., Qu, C., Wang, F., Liu, Y., Qiao, Z., Qiu, X., … Yang, Y. (2015). Using event-related potential P300 as an electrophysiological marker for differential diagnosis and to predict the progression of mild cognitive impairment: A meta-analysis. Neurological Sciences, 36(7), 1105–1112. doi: 10.1007/s10072-015-2099-z.CrossRefGoogle ScholarPubMed
Jimenez-Escrig, A., Fernandez-Lorente, J., Herrero, A., Baron, M., Lousa, M., de Blas, G., & Gobernado, J. (2002). Event-related evoked potential P300 in frontotemporal dementia. Dementia and Geriatric Cognitive Disorders, 13(1), 27–32. doi: 10.1159/000048630.CrossRefGoogle ScholarPubMed
Khedr, E. M., Hamed, S. A., El-Shereef, H. K., Shawky, O. A., Mohamed, K. A., Awad, E. M., … Eltahtawy, M. A. (2009). Cognitive impairment after cerebrovascular stroke: Relationship to vascular risk factors. Neuropsychiatric Disease and Treatment, 5, 103–116. doi: 10.2147/ndt.s4184.Google ScholarPubMed
Kutas, M., McCarthy, G., & Donchin, E. (1977). Augmenting mental chronometry: The P300 as a measure of stimulus evaluation time. Science (New York, N.Y.), 197(4305), 792–795.CrossRefGoogle ScholarPubMed
Linden, D. E. (2005). The p300: Where in the brain is it produced and what does it tell us? Neuroscientist, 11(6), 563–576. doi: 10.1177/1073858405280524.CrossRefGoogle ScholarPubMed
Ludowig, E., Bien, C. G., Elger, C. E., & Rosburg, T. (2010). Two P300 generators in the hippocampal formation. Hippocampus, 20(1), 186–195. doi: 10.1002/hipo.20603.CrossRefGoogle ScholarPubMed
McCarley, R. W., Salisbury, D. F., Hirayasu, Y., Yurgelun-Todd, D. A., Tohen, M., Zarate, C., … Shenton, M. E. (2002). Association between smaller left posterior superior temporal gyrus volume on magnetic resonance imaging and smaller left temporal P300 amplitude in first-episode schizophrenia. Archives of General Psychiatry, 59(4), 321–331.CrossRefGoogle Scholar
McCarley, R. W., Shenton, M. E., O'Donnell, B. F., Faux, S. F., Kikinis, R., Nestor, P. G., & Jolesz, F. A. (1993). Auditory P300 abnormalities and left posterior superior temporal gyrus volume reduction in schizophrenia. Archives of General Psychiatry, 50(3), 190–197.CrossRefGoogle Scholar
Morrison, C., Rabipour, S., Knoefel, F., Sheppard, C., & Taler, V. (2018). Auditory event-related potentials in mild cognitive impairment and Alzheimer's disease. Current Alzheimer Research, 15(8), 702–715. doi: 10.2174/1567205015666180123123209.CrossRefGoogle ScholarPubMed
Morrison, C., Rabipour, S., Taler, V., Sheppard, C., & Knoefel, F. (2019). Visual event-related potentials in mild cognitive impairment and Alzheimer's disease: A literature review. Current Alzheimer Research, 16(1), 67–89. doi: 10.2174/1567205015666181022101036.CrossRefGoogle Scholar
Muller, M. J., Greverus, D., Dellani, P. R., Weibrich, C., Wille, P. R., Scheurich, A., … Fellgiebel, A. (2005). Functional implications of hippocampal volume and diffusivity in mild cognitive impairment. Neuroimage, 28(4), 1033–1042. doi: 10.1016/j.neuroimage.2005.06.029.CrossRefGoogle ScholarPubMed
Petersen, R. C., Jack, C. R., Xu, Y. C., Waring, S. C., O'Brien, P. C., Smith, G. E., … Kokmen, E. (2000). Memory and MRI-based hippocampal volumes in aging and AD. Neurology, 54(3), 581–587.CrossRefGoogle ScholarPubMed
Petersen, R. C., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G., & Kokmen, E. (1999). Mild cognitive impairment: Clinical characterization and outcome. Archives of Neurology, 56(3), 303–308.CrossRefGoogle ScholarPubMed
Polich, J. (2007). Updating P300: An integrative theory of P3a and P3b. Clinical Neurophysiology, 118(10), 2128–2148.CrossRefGoogle ScholarPubMed
Salisbury, D. F., Shenton, M. E., & McCarley, R. W. (1999). P300 topography differs in schizophrenia and manic psychosis. Biological Psychiatry, 45(1), 98–106.CrossRefGoogle ScholarPubMed
Shi, F., Liu, B., Zhou, Y., Yu, C., & Jiang, T. (2009). Hippocampal volume and asymmetry in mild cognitive impairment and Alzheimer's disease: Meta-analyses of MRI studies. Hippocampus, 19(11), 1055–1064. doi: 10.1002/hipo.20573.CrossRefGoogle ScholarPubMed
Silveri, M. C., Reali, G., Jenner, C., & Puopolo, M. (2007). Attention and memory in the preclinical stage of dementia. Journal of Geriatric Psychiatry and Neurology, 20(2), 67–75.CrossRefGoogle ScholarPubMed
Van Dam, N. T., Sano, M., Mitsis, E. M., Grossman, H. T., Gu, X., Park, Y., … Fan, J. (2013). Functional neural correlates of attentional deficits in amnestic mild cognitive impairment. PLoS ONE, 8(1), e54035. doi: 10.1371/journal.pone.0054035.CrossRefGoogle ScholarPubMed
Vandoolaeghe, E., van Hunsel, F., Nuyten, D., & Maes, M. (1998). Auditory event related potentials in major depression: Prolonged P300 latency and increased P200 amplitude. Journal of Affective Disorders, 48(2–3), 105–113.CrossRefGoogle ScholarPubMed
Vinogradova, O. S. (2001). Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus, 11(5), 578–598.CrossRefGoogle ScholarPubMed
Walz, J. M., Goldman, R. I., Carapezza, M., Muraskin, J., Brown, T. R., & Sajda, P. (2014). Simultaneous EEG-fMRI reveals a temporal cascade of task-related and default-mode activations during a simple target detection task. Neuroimage, 102, 229–239. doi: 10.1016/j.neuroimage.2013.08.014.CrossRefGoogle ScholarPubMed
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L. O., … Petersen, R. C. (2004). Mild cognitive impairment – beyond controversies, towards a consensus: Report of the International Working Group on Mild Cognitive Impairment. Journal of Internal Medicine, 256(3), 240–246. doi: 10.1111/j.1365-2796.2004.01380.x.CrossRefGoogle Scholar
Xie, C., Bai, F., Yuan, B., Yu, H., Shi, Y., Yuan, Y., … Zhang, Z. J. (2015). Joint effects of gray matter atrophy and altered functional connectivity on cognitive deficits in amnestic mild cognitive impairment patients. Psychological Medicine, 45(9), 1799–1810. doi: 10.1017/S0033291714002876.CrossRefGoogle ScholarPubMed
Yamaguchi, S., Tsuchiya, H., Yamagata, S., Toyoda, G., & Kobayashi, S. (2000). Event-related brain potentials in response to novel sounds in dementia. Clinical Neurophysiology, 111(2), 195–203.CrossRefGoogle ScholarPubMed
Yang, J., Pan, P., Song, W., Huang, R., Li, J., Chen, K., … Shang, H. (2012). Voxelwise meta-analysis of gray matter anomalies in Alzheimer's disease and mild cognitive impairment using anatomic likelihood estimation. Journal of the Neurological Sciences, 316(1–2), 21–29. doi: 10.1016/j.jns.2012.02.010.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gao et al. supplementary material

Gao et al. supplementary material

Download Gao et al. supplementary material(File)
File 333.6 KB