Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-19T06:05:33.528Z Has data issue: false hasContentIssue false
  • English
  • Français

Three-Dimensional Face Recognition in Mild Cognitive Impairment: A Psychophysical and Structural MR Study

Published online by Cambridge University Press:  13 July 2016

Raquel Lemos ,
Isabel Santana ,
Gina Caetano ,
Inês Bernardino ,
Ricardo Morais ,
Reza Farivar  and
Miguel Castelo-Branco
Raquel Lemos
Affiliation:
Visual Neuroscience Laboratory, Institute of Biomedical Imaging and Life Sciences (CNC.IBILI), IBILI, Faculty of Medicine, University of Coimbra, Coimbra, Portugal Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal
Isabel Santana
Affiliation:
Neurology Department of the Centro Hospitalar Universitário de Coimbra, Coimbra, Portugal
Gina Caetano
Affiliation:
Visual Neuroscience Laboratory, Institute of Biomedical Imaging and Life Sciences (CNC.IBILI), IBILI, Faculty of Medicine, University of Coimbra, Coimbra, Portugal
Inês Bernardino
Affiliation:
Visual Neuroscience Laboratory, Institute of Biomedical Imaging and Life Sciences (CNC.IBILI), IBILI, Faculty of Medicine, University of Coimbra, Coimbra, Portugal
Ricardo Morais
Affiliation:
Neuroradiology Department of the Centro Hospitalar Universitário de Coimbra, Coimbra, Portugal
Reza Farivar
Affiliation:
Harvard Medical School and Massachusetts General Hospital, A. Athinoula Martinos Center for Biomedical Imaging, Charlestown, Massachusetts McGill Vision Research, McGill University, Montreal, Canada
Miguel Castelo-Branco*
Affiliation:
Visual Neuroscience Laboratory, Institute of Biomedical Imaging and Life Sciences (CNC.IBILI), IBILI, Faculty of Medicine, University of Coimbra, Coimbra, Portugal
*
Correspondence and reprint requests to: Miguel Castelo-Branco, Visual Neuroscience Laboratory, IBILI-Faculty of Medicine, University of Coimbra, Azinhaga de Santa Comba, 3000-354 Coimbra, Portugal. E-mail: mcbranco@ibili.uc.pt
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives: Mild cognitive impairment (MCI) has been associated with a high risk of conversion to Alzheimer’s dementia. In addition to memory complaints, impairments in the visuospatial domain have been reported in this condition. We have previously shown that deficits in perceiving structure-from-motion (SFM) objects are reflected in functional reorganization of brain activity within the visual ventral stream. Here we aimed to identify structural correlates of psychophysical complex face and object recognition performance in amnestic MCI patients (n=30 vs. n=25 controls). This study was, therefore, motivated by evidence from recent studies showing that a combination of visual information across dorsal and ventral visual streams may be needed for the perception of three-dimensional (3D) SFM objects. Methods: In our experimental paradigm, participants had to discriminate 3D SFM shapes (faces and objects) from 3D SFM meaningless (scrambled) shapes. Results: Morphometric analysis established neuroanatomical evidence for impairment in MCI as demonstrated by smaller hippocampal volumes. We found association between cortical thickness and face recognition performance, comprising the occipital lobe and visual ventral stream fusiform regions (overlapping the known location of face fusiform area) in the right hemisphere, in MCI. Conclusions: We conclude that impairment of 3D visual integration exists at the MCI stage involving also the visual ventral stream and contributing to face recognition deficits. The specificity of such observed structure-function correlation for faces suggests a special role of this processing pathway in health and disease. (JINS, 2016, 22, 744–754)

Keywords

Mild cognitive impairmentCortical thicknessVisionFusiformDorsal pathwayVentral pathwayStructure-from-motion
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Issue 7 , August 2016 , pp. 744 - 754
Copyright
Copyright © The International Neuropsychological Society 2016 

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

REFERENCES

Albert, M.S., DeKosky, S.T., Dickson, D., Dubois, B., Feldman, H.H., Fox, N.C., & Phelps, C.H. (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. Alzheimer’s & Dementia, 7, 270–279. doi:10.1016/j.jalz.2011.03.008 CrossRefGoogle ScholarPubMed
Bokde, A.L., Lopez-Bayo, P., Born, C., Ewers, M., Meindl, T., Teipel, S.J., &Hampel, H. (2010). Alzheimer disease: Functional abnormalities in the dorsal visual pathway. Radiology, 254, 219–226. doi:10.1148/radiol.2541090558 CrossRefGoogle ScholarPubMed
Bokde, A.L., Lopez-Bayo, P., Meindl, T., Pechler, S., Born, C., Faltraco, F., & Hampel, H. (2006). Functional connectivity of the fusiform gyrus during a face-matching task in subjects with mild cognitive impairment. Brain, 129(Pt 5), 1113–1124. doi:10.1093/brain/awl051 CrossRefGoogle ScholarPubMed
Braddick, O.J., O’Brien, J.M., Wattam-Bell, J., Atkinson, J., & Turner, R. (2000). Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain. Current Biololgy, 10, 731–734. doi:10.1016/S0960-9822(00)00540-6 CrossRefGoogle Scholar
Butter, C.M., Trobe, J.D., Foster, N.L., & Berent, S. (1996). Visual-spatial deficits explain visual symptoms in Alzheimer’s disease. American Journal of Ophthalmology, 122, 97–105. doi:10.1016/S0002-9394(14)71969-5 CrossRefGoogle Scholar
Cabeza, R., & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12, 1–47. doi:10.1162/08989290051137585 CrossRefGoogle Scholar
Castelo-Branco, M., Formisano, E., Backes, W., Zanella, F., Neuenschwander, S., Singer, W., & Goebel, R. (2002). Activity patterns in human motion-sensitive areas depend on the interpretation of global motion. Proceedings of the National Academy of Sciences of the United States of America, 99, 13914–13919. doi:10.1073/pnas.202049999 CrossRefGoogle ScholarPubMed
Castelo-Branco, M., Mendes, M., Silva, F., Massano, J., Januario, G., Januario, C., & Freire, A. (2009). Motion integration deficits are independent of magnocellular impairment in Parkinson’s disease. Neuropsychologia, 47, 314–320. doi:10.1016/j.neuropsychologia.2008.09.003 CrossRefGoogle ScholarPubMed
Castelo-Branco, M., Mendes, M., Silva, M.F., Januario, C., Machado, E., Pinto, A., &Freire, A. (2006). Specific retinotopically based magnocellular impairment in a patient with medial visual dorsal stream damage. Neuropsychologia, 44, 238–253. doi:10.1016/j.neuropsychologia.2005.05.005 CrossRefGoogle Scholar
Cronin-Golomb, A. (2004). Heterogeneity of visual presentation in Alzheimer’s disease. In A. Cronin-Golomb & P.R. Hof (Eds.), Vision in Alzheimer’s disease (Vol. 34, pp. 96–11). Switzerland: Karger.CrossRefGoogle Scholar
Dale, A.M., Fischl, B., & Sereno, M.I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage, 9, 179–194. doi:10.1006/nimg.1998.0395 CrossRefGoogle ScholarPubMed
Desikan, R.S., Segonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., & Killiany, R.J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31, 968–980. doi:10.1016/j.neuroimage.2006.01.021 CrossRefGoogle ScholarPubMed
Dubois, B., Feldman, H.H., Jacova, C., Cummings, J.L., Dekosky, S.T., Barberger-Gateau, P., & Scheltens, P. (2010). Revising the definition of Alzheimer’s disease: A new lexicon. Lancet Neurology, 9, 1118–1127. doi:10.1016/S1474-4422(10)70223-4 CrossRefGoogle ScholarPubMed
Dubois, B., Feldman, H.H., Jacova, C., Dekosky, S.T., Barberger-Gateau, P., Cummings, J., & Scheltens, P. (2007). Research criteria for the diagnosis of Alzheimer’s disease: Revising the NINCDS-ADRDA criteria. Lancet Neurology, 6, 734–746. doi:10.1016/S1474-4422(07)70178-3 CrossRefGoogle ScholarPubMed
Duffy, C.J., Tetewsky, S.J., & O’Brien, H. (2000). Cortical motion blindness in visuospatial AD. Neurobiology of Aging, 21, 867–869. doi:10.1016/S0197-4580(00)00187-1 CrossRefGoogle ScholarPubMed
Farivar, R., Blanke, O., & Chaudhuri, A. (2009). Dorsal-ventral integration in the recognition of motion-defined unfamiliar faces. Journal of Neuroscience, 29, 5336–5342. doi:10.1523/JNEUROSCI.4978-08.2009 CrossRefGoogle ScholarPubMed
Fischl, B., & Dale, A.M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97, 11050–11055. doi:10.1073/pnas.200033797 CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., & Dale, A.M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341–355. doi:10.1016/S0896-6273(02)00569-X CrossRefGoogle ScholarPubMed
Fischl, B., Sereno, M.I., & Dale, A.M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9, 195–207. doi:10.1006/nimg.1998.0396 CrossRefGoogle Scholar
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., & Dale, A.M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11–22.doi:10.1093/cercor/bhg087 CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198. doi:10.1016/0022-3956(75)90026-6 CrossRefGoogle ScholarPubMed
Garrett, C., Santos, F., Tracana, I., Barreto, J., Sobral, M., & Fonseca, R. (2008). Avaliação clínica da demência [Clinical Dementia Rating]. In A. Mendonça, C. Garcia & M. Guerreiro (Eds.), Escalas e testes de demência. [Scales and tests in dementia] Grupo de Estudos de Envelhecimento Cerebral e Demência (pp. 18–32). Lisbon: GEECD. Google Scholar
Graewe, B., Lemos, R., Ferreira, C., Santana, I., Farivar, R., De Weerd, P., & Castelo-Branco, M. (2013). Impaired processing of 3D motion-defined faces in mild cognitive impairment and healthy aging: An fMRI study. Cerebral Cortex, 23, 2489–2499. doi:10.1093/cercor/bhs246 CrossRefGoogle ScholarPubMed
Guerreiro, M. (1998). Contributo da Neuropsicologia para o estudo das demências [Contribution of Neuropsychology to the study of dementia]. (Unpublished doctoral dissertation), University of Lisbon, Lisbon.Google Scholar
Guerreiro, M., Fonseca, S., Barreto, J., & Garcia, C. (2008). Escala de avaliação da doença de Alzheimer - EADA [Alzheimer Disease Assessment Scale- ADAS]. In A. Mendonça, C. Garcia, & M. Guerreiro (Eds.), Escalas e testes de demência. [Scales and tests in dementia] Grupo de Estudos de Envelhecimento Cerebral e Demência (pp. 42–58). Lisbon: GEECD.Google Scholar
Guerreiro, M., Silva, A.P., Botelho, M.A., Leitão, O., Castro-Caldas, A., & Garcia, C. (2008). Avaliação breve do estado mental [Mini Mental State Examination]. In A. Mendonça, C. Garcia, & M. Guerreiro (Eds.), Escalas e testes de demência [Scales and tests in dementia] Grupo de Estudos de Envelhecimento Cerebral e Demência (pp. 33–39). Lisbon: GEECD.Google Scholar
Han, X., Jovicich, J., Salat, D., van der Kouwe, A., Quinn, B., Czanner, S., & Fischl, B. (2006). Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer. Neuroimage, 32, 180–194. doi:10.1016/j.neuroimage.2006.02.051 CrossRefGoogle ScholarPubMed
Jack, C.R. Jr., Bernstein, M.A., Fox, N.C., Thompson, P., Alexander, G., Harvey, D., & Weiner, M.W. (2008). The Alzheimer’s Disease Neuroimaging Initiative (ADNI): MRI methods. Journal of Magnetic Resonance Imaging, 27, 685–691. doi:10.1002/jmri.21049 CrossRefGoogle Scholar
Jacobs, H.I., Gronenschild, E.H., Evers, E.A., Ramakers, I.H., Hofman, P.A., Backes, W.H., & Van Boxtel, M.P. (2012). Visuospatial processing in early Alzheimer’s disease: A multimodal neuroimaging study. Cortex, 64, 394–406. doi:10.1016/j.cortex.2012.01.005 CrossRefGoogle ScholarPubMed
James, T.W., Humphrey, G.K., Gati, J.S., Menon, R.S., & Goodale, M.A. (2002). Differential effects of viewpoint on object-driven activation in dorsal and ventral streams. Neuron, 35, 793–801. doi:10.1016/S0896-6273(02)00803-6 CrossRefGoogle ScholarPubMed
Kavcic, V., Vaughn, W., & Duffy, C.J. (2011). Distinct visual motion processing impairments in aging and Alzheimer’s disease. Vision Research, 51, 386–395. doi:10.1016/j.visres.2010.12.004 CrossRefGoogle ScholarPubMed
Klaver, P., Lichtensteiger, J., Bucher, K., Dietrich, T., Loenneker, T., & Martin, E. (2008). Dorsal stream development in motion and structure-from-motion perception. Neuroimage, 39, 1815–1823. doi:10.1016/j.neuroimage.2007.11.009 CrossRefGoogle ScholarPubMed
Konen, C.S., & Kastner, S. (2008). Two hierarchically organized neural systems for object information in human visual cortex. Nature Neuroscience, 11, 224–231. doi:10.1038/nn2036 CrossRefGoogle ScholarPubMed
Lemos, R., Figueiredo, P., Santana, I., Simoes, M.R., & Castelo-Branco, M. (2012). Temporal integration of 3D coherent motion cues defining visual objects of unknown orientation is impaired in amnestic mild cognitive impairment and Alzheimer’s disease. Journal of Alzheimer’s Disease, 28, 885–896. doi:10.3233/JAD-2011-110719 CrossRefGoogle ScholarPubMed
Levinoff, E.J., Saumier, D., & Chertkow, H. (2005). Focused attention deficits in patients with Alzheimer’s disease and mild cognitive impairment. Brain & Cognition, 57, 127–130. doi:10.1016/j.bandc.2004.08.058 CrossRefGoogle ScholarPubMed
Mapstone, M., Steffenella, T.M., & Duffy, C.J. (2003). A visuospatial variant of mild cognitive impairment: Getting lost between aging and AD. Neurology, 60, 802–808. doi:10.1212/01.WNL.0000049471.76799.DE CrossRefGoogle ScholarPubMed
Mateus, C., Lemos, R., Silva, M.F., Reis, A., Fonseca, P., Oliveiros, B., & Castelo-Branco, M. (2009). Aging of low and high level vision: From chromatic and achromatic contrast sensitivity to local and 3D object motion perception. PLoS One, 8, 1–10. doi:10.1371/journal.pone.0055348 Google Scholar
McKee, A.C., Au, R., Cabral, H.J., Kowall, N.W., Seshadri, S., Kubilus, C.A., & Wolf, P.A. (2006). Visual association pathology in preclinical Alzheimer disease. Journal of Neuropathology and Experimental Neurology, 65, 621–630. doi:10.1097/00005072-200606000-00010 CrossRefGoogle ScholarPubMed
Mendes, M., Silva, F., Simoes, L., Jorge, M., Saraiva, J., & Castelo-Branco, M. (2005). Visual magnocellular and structure from motion perceptual deficits in a neurodevelopmental model of dorsal stream function. Cognitive Brain Research, 25, 788–798. doi:10.1016/j.cogbrainres.2005.09.005 CrossRefGoogle Scholar
Mendola, J.D., Cronin-Golomb, A., Corkin, S., & Growdon, J.H. (1995). Prevalence of visual deficits in Alzheimer’s disease. Optometry and Vision Science, 72, 155–167. doi:10.1097/00006324-199503000-00003 CrossRefGoogle ScholarPubMed
Mentis, M.J., Horwitz, B., Grady, C.L., Alexander, G.E., VanMeter, J.W., Maisog, J.M., & Rapoport, S.I. (1996). Visual cortical dysfunction in Alzheimer’s disease evaluated with a temporally graded “stress test” during PET. American Journal of Psychiatry, 153, 32–40. doi:10.1176/ajp.153.1.32 Google ScholarPubMed
Milner, A.D., & Goodale, M.A. (2008). Two visual systems re-viewed. Neuropsychologia, 46, 774–785. doi:10.1016/j.neuropsychologia.2007.10.005 CrossRefGoogle ScholarPubMed
Mohs, R.C., Rosen, W.G., & Davis, K.L. (1983). The Alzheimer’s disease assessment scale: An instrument for assessing treatment efficacy. Psychopharmacology Bulletin, 19, 448–450.Google ScholarPubMed
Morris, J.C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43, 2412–2414. doi:10.1212/WNL.43.11.2412-a CrossRefGoogle ScholarPubMed
Mysore, S.G., Vogels, R., Raiguel, S.E., Todd, J.T., & Orban, G.A. (2010). The selectivity of neurons in the macaque fundus of the superior temporal area for three-dimensional structure from motion. Journal of Neuroscience, 30, 15491–15508. doi:10.1523/JNEUROSCI.0820-10.2010 CrossRefGoogle ScholarPubMed
Orban, G.A., Sunaert, S., Todd, J.T., Van Hecke, P., & Marchal, G. (1999). Human cortical regions involved in extracting depth from motion. Neuron, 24, 929–940. doi:10.1016/S0896-6273(00)81040-5 CrossRefGoogle ScholarPubMed
Perry, R.J., & Hodges, J.R. (2003). Dissociation between top-down attentional control and the time course of visual attention as measured by attentional dwell time in patients with mild cognitive impairment. European Journal of Neuroscience, 18, 221–226. doi:10.1046/j.1460-9568.2003.02754.x CrossRefGoogle ScholarPubMed
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194. doi:10.1111/j.1365-2796.2004.01388.x CrossRefGoogle ScholarPubMed
Petersen, R.C., Doody, R., Kurz, A., Mohs, R.C., Morris, J.C., Rabins, P.V., & Winblad, B. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992. doi:10.1001/archneur.58.12.1985 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, 303–308. doi:10.1001/archneur.56.3.303 CrossRefGoogle ScholarPubMed
Prvulovic, D., Hubl, D., Sack, A.T., Melillo, L., Maurer, K., Frolich, L., & Dierks, T. (2002). Functional imaging of visuospatial processing in Alzheimer’s disease. Neuroimage, 17, 1403–1414. doi:10.1006/nimg.2002.1271 CrossRefGoogle ScholarPubMed
Reuter-Lorenz, P.A., & Park, D.C. (2014). How does it STAC up? Revisiting the scaffolding theory of aging and cognition. Neuropsychology Review, 24, 355–370. doi:10.1007/s11065-014-9270-9 CrossRefGoogle ScholarPubMed
Risacher, S.L., Wudunn, D., Pepin, S.M., MaGee, T.R., McDonald, B.C., Flashman, L.A., & Saykin, A.J. (2013). Visual contrast sensitivity in Alzheimer’s disease, mild cognitive impairment, and older adults with cognitive complaints. Neurobiology of Aging, 34, 1133–1144. doi:10.1016/j.neurobiolaging.2012.08.007 CrossRefGoogle ScholarPubMed
Rizzo, M., Anderson, S.W., Dawson, J., & Nawrot, M. (2000). Vision and cognition in Alzheimer’s disease. Neuropsychologia, 38, 1157–1169. doi:10.1016/S0028-3932(00)00023-3 CrossRefGoogle ScholarPubMed
Roman, G.C., Tatemichi, T.K., Erkinjuntti, T., Cummings, J.L., Masdeu, J.C., Garcia, J.H., & Hofman, A. (1993). Vascular dementia: Diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology, 43, 250–260. doi:10.1212/WNL.43.2.250 CrossRefGoogle ScholarPubMed
Rose, S.E., McMahon, K.L., Janke, A.L., O’Dowd, B., de Zubicaray, G., Strudwick, M.W., & Chalk, J.B. (2006). Diffusion indices on magnetic resonance imaging and neuropsychological performance in amnestic mild cognitive impairment. Journal of Neurology, Neurosurgery, & Psychiatry, 77, 1122–1128. doi:10.1136/jnnp.2005.074336 CrossRefGoogle ScholarPubMed
Sperling, R. (2011). Potential of functional MRI as a biomarker in early Alzheimer’s disease. Neurobiology of Aging, 32(Suppl. 1), S37–S43. doi:10.1016/j.neurobiolaging.2011.09.009 CrossRefGoogle ScholarPubMed
Tales, A., Haworth, J., Nelson, S., Snowden, R.J., & Wilcock, G. (2005). Abnormal visual search in mild cognitive impairment and Alzheimer’s disease. Neurocase, 11, 80–84. doi:10.1080/13554790490896974 CrossRefGoogle ScholarPubMed
Teipel, S.J., Bokde, A.L., Born, C., Meindl, T., Reiser, M., Möller, H.J., & Hampel, H. (2007). Morphological substrate of face matching in healthy ageing and mild cognitive impairment: A combined MRI-fMRI study. Brain, 130, 1745–1758. doi:10.1093/brain/awm117 CrossRefGoogle ScholarPubMed
Teipel, S.J., Grothe, M., Lista, S., Toschi, N., Garaci, F.G., & Hampel, H. (2013). Relevance of magnetic resonance imaging for early detection and diagnosis of Alzheimer disease. Medical Clinics of North America, 97, 399–424. doi:10.1016/j.mcna.2012.12.013 CrossRefGoogle ScholarPubMed
Troje, N.F., & Bulthoff, H.H. (1996). Face recognition under varying poses: The role of texture and shape. Vision Research, 36, 1761–1771. doi:10.1016/0042-6989(95)00230-8 CrossRefGoogle ScholarPubMed
Vannini, P., Almkvist, O., Dierks, T., Lehmann, C., & Wahlund, L.O. (2007). Reduced neuronal efficacy in progressive mild cognitive impairment: A prospective fMRI study on visuospatial processing. Psychiatry Research, 156, 43–57. doi:10.1016/j.pscychresns.2007.02.003 CrossRefGoogle Scholar
Villain, N., Chetelat, G., Desgranges, B., & Eustache, F. (2010). Neuroimaging in Alzheimer’s disease: A synthesis and a contribution to the understanding of physiopathological mechanisms. Biologie Aujourdhui, 204, 145–158. doi:10.1051/jbio/2010010 CrossRefGoogle Scholar
Villain, N., Fouquet, M., Baron, J.C., Mezenge, F., Landeau, B., de La Sayette, V., & Chételat, G. (2010). Sequential relationships between grey matter and white matter atrophy and brain metabolic abnormalities in early Alzheimer’s disease. Brain, 133, 3301–3314. doi:10.1093/brain/awq203 CrossRefGoogle ScholarPubMed
Xiao, D.K., Marcar, V.L., Raiguel, S.E., & Orban, G.A. (1997). Selectivity of macaque MT/V5 neurons for surface orientation in depth specified by motion. European Journal of Neuroscience, 9, 956–964. doi:10.1111/j.1460-9568.1997.tb01446.x CrossRefGoogle ScholarPubMed
Yamasaki, T., Muranaka, H., Kaseda, Y., Mimori, Y., & Tobimatsu, S. (2012). Understanding the pathophysiology of Alzheimer’s disease and mild cognitive impairment: A mini review on fMRI and ERP studies. Neurology Research International, 2012, 1–10. doi:10.1155/2012/719056 CrossRefGoogle ScholarPubMed