Altered Frontal Lateralization Underlies the Category Fluency Deficits in Older Adults with Mild Cognitive Impairment: A Near-Infrared Spectroscopy Study

Michael K Yeung, Sophia L Sze, Jean Woo, Timothy Kwok, David H K Shum, Ruby Yu, Agnes S Chan, Michael K Yeung, Sophia L Sze, Jean Woo, Timothy Kwok, David H K Shum, Ruby Yu, Agnes S Chan

Abstract

Individuals with mild cognitive impairment (MCI) have been consistently found to have category fluency deficits. However, little is known about the neural basis of these deficits. A diversity of neuroimaging studies has revealed left-lateralized prefrontal activations due to verbal processing and control functions during the performance of category fluency tasks. Given the reports of structural and functional abnormalities in the prefrontal cortices in individuals with MCI, it is conceivable that these individuals would also exhibit altered prefrontal activation patterns during a category fluency task. The present study aimed to investigate the prefrontal dynamics during the category fluency task in older adults with MCI by using near-infrared spectroscopy (NIRS). Twenty-six older adults with MCI were compared with 26 older adults with normal cognition (NC) who were matched in age, gender, handedness, and educational level. All participants performed a category fluency task while the prefrontal dynamics were recorded. The results showed that the MCI group generated fewer unique words, made fewer switches between subcategories, and generated fewer new subcategories than did the NC group. Importantly, the NIRS results showed that the NC group exhibited a left lateralization of frontal activations during the category fluency task, while the MCI group did not exhibit such a lateralization. Furthermore, there was a significant positive correlation between the category fluency performance and the extent of lateralization, suggesting that the category fluency deficits in the MCI group could be related to frontal dysfunction. That is, the rightward shift of frontal activations in the MCI group may reflect the presence of cortical reorganization in which the contralateral regions (i.e., the right hemisphere) are recruited to take over the function that is declining in the specialized regions (i.e., the left hemisphere). Our lateralization finding may serve as an objective neural marker for distinguishing between normal aging and MCI. Our study highlights that an alteration of neural functioning is already present at the prodromal stage of dementia.

Keywords: category fluency; lateralization; mild cognitive impairment (MCI); near-infrared spectroscopy (NIRS); prefrontal cortex; verbal fluency.

Figures

Figure 1
Figure 1
Arrangement of the near-infrared spectroscopy (NIRS) channels. Channels 13–16 represent the left prefrontal region, and channels 1–4 represent the right prefrontal region. The distance between pairs of emitter and detector probes was 3 cm. In accordance to the international 10/20 system, the center of the probe matrix was placed on Fpz, and the probes at the bottom left and right corners were placed around F7 and F8, respectively.
Figure 2
Figure 2
The laterality index of the mean [oxy-Hb] changes at the lateral prefrontal regions in the mild cognitive impairment (MCI; n = 26) and normal cognition (NC; n = 26) groups. A positive value implies a lateralization to the left, whereas a negative value implies a lateralization to the right. No outliers (i.e., two SDs above or below the group mean) were identified. **p < 0.01.
Figure 3
Figure 3
Mean [oxy-Hb] changes at the left (ch13–16) and right (ch1–4) prefrontal regions during the category fluency tasks in the MCI (n = 26) and NC (n = 26) groups. Error bars denote the 95% confidence interval. *p < 0.05.
Figure 4
Figure 4
The relationship between the laterality index and total unique words generated in 60 s in the MCI (n = 26) and NC (n = 26) groups. A linear regression line was fit for each group separately.
Figure 5
Figure 5
The laterality index of the [oxy-Hb] changes at the lateral prefrontal regions in the amnestic (aMCI; n = 10) and non-amnestic MCI (naMCI; n = 16) and NC (n = 26) groups. A positive value implies a lateralization to the left, whereas a negative value implies a lateralization to the right. No outliers (i.e., 2 SDs above or below the group mean) were identified. †p < 0.10; **p < 0.01.

References

    1. Ahn H., Seo S. W., Chin J., Suh M. K., Lee B. H., Kim S. T., et al. . (2011). The cortical neuroanatomy of neuropsychological deficits in mild cognitive impairment and Alzheimer’s disease: a surface-based morphometric analysis. Neuropsychologia 49, 3931–3945. 10.1016/j.neuropsychologia.2011.10.010
    1. Albert M. S., DeKosky S. T., Dickson D., Dubois B., Feldman H. H., Fox N. C., et al. . (2011). 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. Alzheimers Dement. 7, 270–279. 10.1016/j.jalz.2011.03.008
    1. Alichniewicz K. K., Brunner F., Klünemann H. H., Greenlee M. W. (2012). Structural and functional neural correlates of visuospatial information processing in normal aging and amnestic mild cognitive impairment. Neurobiol. Aging 33, 2782–2797. 10.1016/j.neurobiolaging.2012.02.010
    1. Amieva H., Letenneur L., Dartigues J. F., Rouch-Leroyer I., Sourgen C., D’Alchée-Birée F., et al. . (2004). Annual rate and predictors of conversion to dementia in subjects presenting mild cognitive impairment criteria defined according to a population-based study. Dement. Geriatr. Cogn. Disord. 18, 87–93. 10.1159/000077815
    1. Badre D., Wagner A. D. (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia 45, 2883–2901. 10.1016/j.neuropsychologia.2007.06.015
    1. Beck A. T., Epstein N., Brown G., Steer R. A. (1988). An inventory for measuring clinical anxiety: psychometric properties. J. Consult. Clin. Psychol. 56, 893–897. 10.1037/0022-006x.56.6.893
    1. Bernstein J. H., Waber D. P. (1996). Developmental Scoring System for the Rey-Osterrieth Complex Figure. Odessa, FL: Psychological Assessment Resources.
    1. Bertola L., Lima M. L. C., Romano-Silva M. A., de Moraes E. N., Diniz B. S., Malloy-Diniz L. F. (2014). Impaired generation of new subcategories and switching in a semantic verbal fluency test in older adults with mild cognitive impairment. Front. Aging Neurosci. 6:141. 10.3389/fnagi.2014.00141
    1. Birn R. M., Kenworthy L., Case L., Caravella R., Jones T. B., Bandettini P. A., et al. . (2010). Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency. Neuroimage 49, 1099–1107. 10.1016/j.neuroimage.2009.07.036
    1. Bondi M. W., Edmonds E. C., Jak A. J., Clark L. R., Delano-Wood L., McDonald C. R., et al. . (2014). Neuropsychological criteria for mild cognitive impairment improves diagnostic precision, biomarker associations and progression rates. J. Alzheimers Dis. 42, 275–289. 10.3233/JAD-140276
    1. Brandt J., Manning K. J. (2009). Patterns of word-list generation in mild cognitive impairment and Alzheimer’s disease. Clin. Neuropsychol. 23, 870–879. 10.1080/13854040802585063
    1. Chan A. S., Choi M. K., Salmon D. P. (2001). The effects of age, education and gender on the mattis dementia rating scale performance of elderly chinese and american individuals. J. Gerontol. B Psychol. Sci. Soc. Sci. 56, P356–P363. 10.1093/geronb/56.6.p356
    1. Chan A. S., Kwok I. (2006). Hong Kong List Learning Test. 2nd Edn. Hong Kong: Department of Psychological and Integrative Neuropsychological Rehabilitation Center.
    1. Chan A. S., Poon M. W. (1999). Performance of 7-to 95-year-old individuals in a chinese version of the category fluency test. J. Int. Neuropsychol. Soc. 5, 525–533. 10.1017/s135561779956606x
    1. Chang Y.-L., Jacobson M. W., Fennema-Notestine C., Hagler D. J., Jr., Jennings R. G., Dale A. M., et al. . (2010). Level of executive function influences verbal memory in amnestic mild cognitive impairment and predicts prefrontal and posterior cingulate thickness. Cereb. Cortex 20, 1305–1313. 10.1093/cercor/bhp192
    1. Chao L. L., Pa J., Duarte A., Schuff N., Weiner M. W., Kramer J. H., et al. . (2009). Patterns of cerebral hypoperfusion in amnestic and dysexecutive MCI. Alzheimer Dis. Assoc. Disord. 23, 245–252. 10.1097/WAD.0b013e318199ff46
    1. Chaudhary U., Hall M., DeCerce J., Rey G., Godavarty A. (2011). Frontal activation and connectivity using near-infrared spectroscopy: verbal fluency language study. Brain Res. Bull. 84, 197–205. 10.1016/j.brainresbull.2011.01.002
    1. Cheung R. W., Cheung M., Chan A. S. (2004). Confrontation naming in chinese patients with left, right or bilateral brain damage. J. Int. Neuropsychol. Soc. 10, 46–53. 10.1017/s1355617704101069
    1. Clark L. R., Delano-Wood L., Libon D. J., McDonald C. R., Nation D. A., Bangen K. J., et al. . (2013). Are empirically-derived subtypes of mild cognitive impairment consistent with conventional subtypes? J. Int. Neuropsychol. Soc. 19, 635–645. 10.1017/s1355617713000313
    1. Clark D., Wadley V., Kapur P., DeRamus T., Singletary B., Nicholas A., et al. . (2014). Lexical factors and cerebral regions influencing verbal fluency performance in MCI. Neuropsychologia 54, 98–111. 10.1016/j.neuropsychologia.2013.12.010
    1. Cui X., Bray S., Bryant D. M., Glover G. H., Reiss A. L. (2011). A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. Neuroimage 54, 2808–2821. 10.1016/j.neuroimage.2010.10.069
    1. Dan H., Dan I., Sano T., Kyutoku Y., Oguro K., Yokota H., et al. . (2013). Language-specific cortical activation patterns for verbal fluency tasks in japanese as assessed by multichannel functional near-infrared spectroscopy. Brain Lang. 126, 208–216. 10.1016/j.bandl.2013.05.007
    1. Dannhauser T. M., Walker Z., Stevens T., Lee L., Seal M., Shergill S. S. (2005). The functional anatomy of divided attention in amnestic mild cognitive impairment. Brain 128, 1418–1427. 10.1093/brain/awh413
    1. de Guibert C., Maumet C., Jannin P., Ferré J., Tréguier C., Barillot C., et al. . (2011). Abnormal functional lateralization and activity of language brain areas in typical specific language impairment (developmental dysphasia). Brain 134, 3044–3058. 10.1093/brain/awr141
    1. Delpy D. T., Cope M., van der Zee P., Arridge S. R., Wray S., Wyatt J. S. (1988). Estimation of optical pathlength through tissue from direct time of flight measurement. Phys. Med. Biol. 33, 1433–1442. 10.1088/0031-9155/33/12/008
    1. Eastman J. A., Hwang K. S., Lazaris A., Chow N., Ramirez L., Babakchanian S., et al. . (2013). Cortical thickness and semantic fluency in Alzheimer’s disease and mild cognitive impairment. Am. J. Alzheimers Dis. (Columbia) 1, 81–92. 10.7726/ajad.2013.1006
    1. Ehlis A., Herrmann M. J., Plichta M. M., Fallgatter A. J. (2007). Cortical activation during two verbal fluency tasks in schizophrenic patients and healthy controls as assessed by multi-channel near-infrared spectroscopy. Psychiatry Res. 156, 1–13. 10.1016/j.pscychresns.2006.11.007
    1. Ernst R. L., Hay J. W., Fenn C., Tinklenberg J., Yesavage J. A. (1997). Cognitive function and the costs of Alzheimer disease: an exploratory study. Arch. Neurol. 54, 687–693. 10.1001/archneur.1997.00550180013006
    1. Fallgatter A., Roesler M., Sitzmann A., Heidrich A., Mueller T., Strik W. (1997). Loss of functional hemispheric asymmetry in Alzheimer’s dementia assessed with near-infrared spectroscopy. Brain Res. Cogn. Brain Res. 6, 67–72. 10.1016/s0926-6410(97)00016-5
    1. Galasko D., Bennett D. A., Sano M., Marson D., Kaye J., Edland S. D. (2006). ADCS prevention instrument project: assessment of instrumental activities of daily living for community-dwelling elderly individuals in dementia prevention clinical trials. Alzheimer Dis. Assoc. Disord. 20, S152–S169. 10.1097/01.wad.0000213873.25053.2b
    1. Gourovitch M. L., Kirkby B. S., Goldberg T. E., Weinberger D. R., Gold J. M., Esposito G., et al. . (2000). A comparison of rCBF patterns during letter and semantic fluency. Neuropsychology 14, 353–360. 10.1037/0894-4105.14.3.353
    1. Gutierrez-Sigut E., Payne H., MacSweeney M. (2015). Investigating language lateralization during phonological and semantic fluency tasks using functional transcranial doppler sonography. Laterality 20, 49–68. 10.1080/1357650x.2014.914950
    1. Heinzel S., Metzger F. G., Ehlis A., Korell R., Alboji A., Haeussinger F. B., et al. . (2013). Aging-related cortical reorganization of verbal fluency processing: a functional near-infrared spectroscopy study. Neurobiol. Aging 34, 439–450. 10.1016/j.neurobiolaging.2012.05.021
    1. Heinzel S., Metzger F. G., Ehlis A., Korell R., Alboji A., Haeussinger F. B., et al. . (2015). Age and vascular burden determinants of cortical hemodynamics underlying verbal fluency. PLoS One 10:e0138863. 10.1371/journal.pone.0138863
    1. Hellige J. B. (1993). Hemispheric Asymmetry: What’s Right and What’s Left. Cambridge, MA: Harvard University Press.
    1. Heun R., Freymann K., Erb M., Leube D. T., Jessen F., Kircher T. T., et al. . (2007). Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly. Neurobiol. Aging 28, 404–413. 10.1016/j.neurobiolaging.2006.01.012
    1. Holper L., Aleksandrowicz A., Müller M., Ajdacic-Gross V., Haker H., Fallgatter A., et al. . (2015). Brain correlates of verbal fluency in subthreshold psychosis assessed by functional near-infrared spectroscopy. Schizophr. Res. 168, 23–29. 10.1016/j.schres.2015.07.043
    1. Hori H., Ozeki Y., Terada S., Kunugi H. (2008). Functional near-infrared spectroscopy reveals altered hemispheric laterality in relation to schizotypy during verbal fluency task. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1944–1951. 10.1016/j.pnpbp.2008.09.019
    1. Jak A. J., Bondi M. W., Delano-Wood L., Wierenga C., Corey-Bloom J., Salmon D. P., et al. . (2009). Quantification of five neuropsychological approaches to defining mild cognitive impairment. Am. J. Geriatr. Psychiatry 17, 368–375. 10.1097/JGP.0b013e31819431d5
    1. Jasper H. H. (1958). The 10/20 international electrode system. Electroencephalogr. Clin. Neurophysiol. 10, 371–375.
    1. Kahlaoui K., Di Sante G., Barbeau J., Maheux M., Lesage F., Ska B., et al. . (2012). Contribution of NIRS to the study of prefrontal cortex for verbal fluency in aging. Brain Lang. 121, 164–173. 10.1016/j.bandl.2011.11.002
    1. Kaufmann L., Ischebeck A., Weiss E., Koppelstaetter F., Siedentopf C., Vogel S. E., et al. . (2008). An fMRI study of the numerical stroop task in individuals with and without minimal cognitive impairment. Cortex 44, 1248–1255. 10.1016/j.cortex.2007.11.009
    1. Kubota Y., Toichi M., Shimizu M., Mason R. A., Coconcea C. M., Findling R. L., et al. . (2005). Prefrontal activation during verbal fluency tests in schizophrenia—a near-infrared spectroscopy (NIRS) study. Schizophr. Res. 77, 65–73. 10.1016/j.schres.2005.01.007
    1. Lee H. B., Chiu H. F., Kowk W. Y., Leung C. M. (1993). Chinese elderly and the GDS short form: a preliminary study. Clin. Gerontol. J. Aging Ment. Health 14, 37–42.
    1. Li H., Hou X., Liu H., Yue C., He Y., Zuo X. (2015). Toward systems neuroscience in mild cognitive impairment and Alzheimer’s disease: a meta-analysis of 75 fMRI studies. Hum. Brain Mapp. 36, 1217–1232. 10.1002/hbm.22689
    1. Libon D. J., Xie S. X., Eppig J., Wicas G., Lamar M., Lippa C., et al. . (2010). The heterogeneity of mild cognitive impairment: a neuropsychological analysis. J. Int. Neuropsychol. Soc. 16, 84–93. 10.1017/s1355617709990993
    1. Liu X., Sun G., Zhang X., Xu B., Shen C., Shi L., et al. . (2014). Relationship between the prefrontal function and the severity of the emotional symptoms during a verbal fluency task in patients with major depressive disorder: a multi-channel NIRS study. Prog. Neuropsychopharmacol. Biol. Psychiatry 54, 114–121. 10.1016/j.pnpbp.2014.05.005
    1. Makizako H., Doi T., Shimada H., Park H., Uemura K., Yoshida D., et al. . (2013). Relationship between going outdoors daily and activation of the prefrontal cortex during verbal fluency tasks (VFTs) among older adults: a near-infrared spectroscopy study. Arch. Gerontol. Geriatr. 56, 118–123. 10.1016/j.archger.2012.08.017
    1. Marumo K., Takizawa R., Kinou M., Kawasaki S., Kawakubo Y., Fukuda M., et al. . (2014). Functional abnormalities in the left ventrolateral prefrontal cortex during a semantic fluency task and their association with thought disorder in patients with schizophrenia. Neuroimage 85, 518–526. 10.1016/j.neuroimage.2013.04.050
    1. Meinzer M., Flaisch T., Wilser L., Eulitz C., Rockstroh B., Conway T., et al. (2009). Neural signatures of semantic and phonemic fluency in young and old adults. J. Cogn. Neurosci. 21, 2007–2018. 10.1162/jocn.2009.21219
    1. Meinzer M., Lindenberg R., Antonenko D., Flaisch T., Floel A. (2013). Anodal transcranial direct current stimulation temporarily reverses age-associated cognitive decline and functional brain activity changes. J. Neurosci. 33, 12470–12478. 10.1523/JNEUROSCI.5743-12.2013
    1. Molinuevo J. L., Gómez-Anson B., Monte G. C., Bosch B., Sánchez-Valle R., Rami L. (2011). Neuropsychological profile of prodromal Alzheimer’s disease (prd-AD) and their radiological correlates. Arch. Gerontol. Geriatr. 52, 190–196. 10.1016/j.archger.2010.03.016
    1. Murphy K. J., Rich J. B., Troyer A. K. (2006). Verbal fluency patterns in amnestic mild cognitive impairment are characteristic of Alzheimer’s type dementia. J. Int. Neuropsychol. Soc. 12, 570–574. 10.1017/s1355617706060590
    1. Nutter-Upham K. E., Saykin A. J., Rabin L. A., Roth R. M., Wishart H. A., Pare N., et al. . (2008). Verbal fluency performance in amnestic MCI and older adults with cognitive complaints. Arch. Clin. Neuropsychol. 23, 229–241. 10.1016/j.acn.2008.01.005
    1. Pa J., Boxer A., Chao L. L., Gazzaley A., Freeman K., Kramer J., et al. . (2009). Clinical-neuroimaging characteristics of dysexecutive mild cognitive impairment. Ann. Neurol. 65, 414–423. 10.1002/ana.21591
    1. Papma J. M., den Heijer T., de Koning I., Mattace-Raso F. U., van der Lugt A., van der Lijn F., et al. . (2013). The influence of cerebral small vessel disease on default mode network deactivation in mild cognitive impairment. Neuroimage Clin. 2, 33–42. 10.1016/j.nicl.2012.11.005
    1. Petersen R., Caracciolo B., Brayne C., Gauthier S., Jelic V., Fratiglioni L. (2014). Mild cognitive impairment: a concept in evolution. J. Intern. Med. 275, 214–228. 10.1111/joim.12190
    1. 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. Arch. Neurol. 56, 303–308. 10.1001/archneur.56.3.303
    1. Price S. E., Kinsella G. J., Ong B., Storey E., Mullaly E., Phillips M., et al. . (2012). Semantic verbal fluency strategies in amnestic mild cognitive impairment. Neuropsychology 26, 490–497. 10.1037/a0028567
    1. Raja Beharelle A., Dick A. S., Josse G., Solodkin A., Huttenlocher P. R., Levine S. C., et al. . (2010). Left hemisphere regions are critical for language in the face of early left focal brain injury. Brain 133, 1707–1716. 10.1093/brain/awQ114
    1. Raoux N., Amieva H., Le Goff M., Auriacombe S., Carcaillon L., Letenneur L., et al. . (2008). Clustering and switching processes in semantic verbal fluency in the course of Alzheimer’s disease subjects: results from the PAQUID longitudinal study. Cortex 44, 1188–1196. 10.1016/j.cortex.2007.08.019
    1. Rinehardt E., Eichstaedt K., Schinka J. A., Loewenstein D. A., Mattingly M., Fils J., et al. . (2014). Verbal fluency patterns in mild cognitive impairment and Alzheimer’s disease. Dement. Geriatr. Cogn. Disord. 38, 1–9. 10.1159/000355558
    1. Sato H., Yahata N., Funane T., Takizawa R., Katura T., Atsumori H., et al. . (2013). A NIRS-fMRI investigation of prefrontal cortex activity during a working memory task. Neuroimage 83, 158–173. 10.1016/j.neuroimage.2013.06.043
    1. Schecklmann M., Ehlis A., Plichta M. M., Boutter H. K., Metzger F. G., Fallgatter A. J. (2007). Altered frontal brain oxygenation in detoxified alcohol dependent patients with unaffected verbal fluency performance. Psychiatry Res. 156, 129–138. 10.1016/j.pscychresns.2007.01.009
    1. Seghier M. L. (2008). Laterality index in functional MRI: methodological issues. Magn. Reson. Imaging 26, 594–601. 10.1016/j.mri.2007.10.010
    1. Simons J. S., Spiers H. J. (2003). Prefrontal and medial temporal lobe interactions in long-term memory. Nat. Rev. Neurosci. 4, 637–648. 10.1038/nrn1178
    1. Sommer I. E. C., Ramsey N. F., Kahn R. S. (2001). Language lateralization in schizophrenia, an fMRI study. Schizophr. Res. 52, 57–67. 10.1016/s0920-9964(00)00180-8
    1. Strangman G., Culver J. P., Thompson J. H., Boas D. A. (2002). A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 17, 719–731. 10.1006/nimg.2002.1227
    1. Stuss D. T., Knight R. T. (2013). Principles of Frontal Lobe Function. New York, NY: Oxford University Press.
    1. Thompson-Schill S. L., D’Esposito M., Aguirre G. K., Farah M. J. (1997). Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc. Natl. Acad. Sci. U S A 94, 14792–14797. 10.1073/pnas.94.26.14792
    1. Tierney M. C., Yao C., Kiss A., McDowell I. (2005). Neuropsychological tests accurately predict incident Alzheimer disease after 5 and 10 years. Neurology 64, 1853–1859. 10.1212/01.WNL.0000163773.21794.0B
    1. Troyer A. K. (2000). Normative data for clustering and switching on verbal fluency tasks. J. Clin. Exp. Neuropsychol. 22, 370–378. 10.1076/1380-3395(200006)22:3;1-v;ft370
    1. Tupak S. V., Badewien M., Dresler T., Hahn T., Ernst L. H., Herrmann M. J., et al. . (2012). Differential prefrontal and frontotemporal oxygenation patterns during phonemic and semantic verbal fluency. Neuropsychologia 50, 1565–1569. 10.1016/j.neuropsychologia.2012.03.009
    1. Van Dam N. T., Sano M., Mitsis E. M., Grossman H. T., Gu X., Park Y., et al. . (2013). Functional neural correlates of attentional deficits in amnestic mild cognitive impairment. PLoS One 8:e54035. 10.1371/journal.pone.0054035
    1. Venneri A., Gorgoglione G., Toraci C., Nocetti L., Panzetti P., Nichelli P. (2011). Combining neuropsychological and structural neuroimaging indicators of conversion to Alzheimer’s disease in amnestic mild cognitive impairment. Curr. Alzheimer Res. 8, 789–797. 10.2174/156720511797633160
    1. Villringer A., Chance B. (1997). Non-invasive optical spectroscopy and imaging of human brain function. Trends Neurosci. 20, 435–442. 10.1016/S0166-2236(97)01132-6
    1. Vogel A., Johannsen P., Stokholm J., Jørgensen K. (2014). Frequency and severity of semantic deficits in a consecutive memory clinic cohort. Dement. Geriatr. Cogn. Disord. 38, 214–223. 10.1159/000357794
    1. Wagner S., Sebastian A., Lieb K., Tüscher O., Tadić A. (2014). A coordinate-based ALE functional MRI meta-analysis of brain activation during verbal fluency tasks in healthy control subjects. BMC Neurosci. 15:19. 10.1186/1471-2202-15-19
    1. Wang L., Goldstein F. C., Veledar E., Levey A. I., Lah J. J., Meltzer C. C., et al. . (2009). Alterations in cortical thickness and white matter integrity in mild cognitive impairment measured by whole-brain cortical thickness mapping and diffusion tensor imaging. AJNR Am. J. Neuroradiol. 30, 893–899. 10.3174/ajnr.a1484
    1. Wang P.-N., Hong C.-J., Lin K.-N., Liu H.-C., Chen W.-T. (2011). APOE ɛ4 increases the risk of progression from amnestic mild cognitive impairment to Alzheimer’s disease among ethnic chinese in taiwan. J. Neurol Neurosurg. Psychiatry 82, 165–169. 10.1136/jnnp.2010.209122
    1. Weakley A., Schmitter-Edgecombe M., Anderson J. (2013). Analysis of verbal fluency ability in amnestic and non-amnestic mild cognitive impairment. Arch. Clin. Neuropsychol. 28, 721–731. 10.1093/arclin/act058
    1. Wechsler D. (2005). Wechsler Memory Scale III (Chinese): Manual. Taiwan: Psychological Corporation.
    1. Weiss E. M., Hofer A., Golaszewski S., Siedentopf C., Brinkhoff C., Kremser C., et al. . (2004). Brain activation patterns during a verbal fluency test—a functional MRI study in healthy volunteers and patients with schizophrenia. Schizophr. Res. 70, 287–291. 10.1016/j.schres.2004.01.010
    1. Weiss E., Siedentopf C., Hofer A., Deisenhammer E., Hoptman M., Kremser C., et al. . (2003). Brain activation pattern during a verbal fluency test in healthy male and female volunteers: a functional magnetic resonance imaging study. Neurosci. Lett. 352, 191–194. 10.1016/j.neulet.2003.08.071
    1. Woodard J. L., Seidenberg M., Nielson K. A., Antuono P., Guidotti L., Durgerian S., et al. . (2009). Semantic memory activation in amnestic mild cognitive impairment. Brain 132, 2068–2078. 10.1093/brain/awp157
    1. Yaffe K., Petersen R. C., Lindquist K., Kramer J., Miller B. (2006). Subtype of mild cognitive impairment and progression to dementia and death. Dement. Geriatr. Cogn. Disord. 22, 312–319. 10.1159/000095427
    1. Yeung M. K., Han Y. M., Sze S. L., Chan A. S. (2016). Abnormal frontal theta oscillations underlie the cognitive flexibility deficits in children with high-functioning autism spectrum disorders. Neuropsychology 30, 281–295. 10.1037/neu0000231
    1. Zhao Q., Guo Q., Li F., Zhou Y., Wang B., Hong Z. (2013). The shape trail test: application of a new variant of the trail making test. PLoS One 8:e57333. 10.1371/journal.pone.0057333
    1. Zhao H., Li X., Wu W., Li Z., Qian L., Li S., et al. . (2015). Atrophic patterns of the frontal-subcortical circuits in patients with mild cognitive impairment and Alzheimer’s disease. PLoS One 10:e0130017. 10.1371/journal.pone.0130017

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅