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Cognitive reserve lessens the burden of white matter lesions on executive functions in bipolar disorder

Published online by Cambridge University Press:  18 August 2016

S. Rolstad ,
C. Abé ,
E. Olsson ,
C. Eckerström  and
M. Landén
S. Rolstad*
Affiliation:
Institute of Neuroscience and Physiology, Sahlgrenska Academy at Gothenburg University, Gothenburg, Sweden
C. Abé
Affiliation:
Department of Clinical Neuroscience, Osher Center, Karolinska Institutet, Stockholm, Sweden
E. Olsson
Affiliation:
Institute of Neuroscience and Physiology, Sahlgrenska Academy at Gothenburg University, Gothenburg, Sweden
C. Eckerström
Affiliation:
Institute of Neuroscience and Physiology, Sahlgrenska Academy at Gothenburg University, Gothenburg, Sweden
M. Landén
Affiliation:
Institute of Neuroscience and Physiology, Sahlgrenska Academy at Gothenburg University, Gothenburg, Sweden Department of Clinical Neuroscience, Osher Center, Karolinska Institutet, Stockholm, Sweden Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden
*
*Address for correspondence: S. Rolstad, Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, Sahlgrenska Academy at University of Gothenburg, Blå stråket 15, SE-413 45 Gothenburg, Sweden. (Email: [email protected])
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Abstract

Background

The concept of cognitive reserve (CR) hypothesizes that intellectually stimulating activities provide resilience against brain pathology/disease. Whereas brain abnormalities and cognitive impairment are frequently reported in bipolar disorder (BD), it is unknown whether the impact of brain alterations can be lessened by higher CR in BD.

Method

We tested if higher CR would reduce the influence of total volumes of deep white matter hypointensities (WMH), ventricular cerebrospinal fluid (CSF), and prefrontal cortex on memory, executive, and attention/speed functions in patients with BD (n = 75). Linear regression models with interaction terms for CR and brain volumes were applied to directly test if CR reduces the influence of brain pathology on cognitive domains.

Results

CR reduced the influence of total volumes of deep WMH (β = −0.38, Q = 0.003) and ventricular CSF (β = −41, Q = 006) on executive functions.

Conclusions

The interactions between CR and total volumes of deep WMH/ventricular CSF appear to account for executive functioning in BD. The results suggest that the concept of CR is applicable in BD. Higher reserve capacity in BD alters the relationship between brain pathology and clinical presentation.

Keywords

Bipolar disordercognitioncognitive reservemagnetic resonance imaging
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 15 , November 2016 , pp. 3095 - 3104
Copyright
Copyright © Cambridge University Press 2016 

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References

Abe, C, Ekman, CJ, Sellgren, C, Petrovic, P, Ingvar, M, Landen, M (2016). Cortical thickness, volume and surface area in patients with bipolar disorder types I and II. Journal of Psychiatry and Neuroscience 41, 240–250.CrossRefGoogle ScholarPubMed
Ahearn, EP, Steffens, DC, Cassidy, F, Van Meter, SA, Provenzale, JM, Seldin, MF, Weisler, RH, Krishnan, KR (1998). Familial leukoencephalopathy in bipolar disorder. American Journal of Psychiatry 155, 1605–1607.CrossRefGoogle ScholarPubMed
Alchanatis, M, Zias, N, Deligiorgis, N, Amfilochiou, A, Dionellis, G, Orphanidou, D (2005). Sleep apnea-related cognitive deficits and intelligence: an implication of cognitive reserve theory. Journal of Sleep Research 14, 69–75.CrossRefGoogle ScholarPubMed
Alexander, GE, Furey, ML, Grady, CL, Pietrini, P, Brady, DR, Mentis, MJ, Schapiro, MB (1997). Association of premorbid intellectual function with cerebral metabolism in Alzheimer's disease: implications for the cognitive reserve hypothesis. American Journal of Psychiatry 154, 165–172.Google ScholarPubMed
Alosco, ML, Spitznagel, MB, Raz, N, Cohen, R, Sweet, LH, Van Dulmen, M, Colbert, LH, Josephson, R, Waechter, D, Hughes, J, Rosneck, J, Gunstad, J (2012). Cognitive reserve moderates the association between heart failure and cognitive impairment. Journal of Clinical and Experimental Neuropsychology 34, 1–10.CrossRefGoogle ScholarPubMed
American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. DSM-IV-TR®. American Psychiatric Association: Washington, DC.Google Scholar
Arnone, D, Cavanagh, J, Gerber, D, Lawrie, SM, Ebmeier, KP, Mcintosh, AM (2009). Magnetic resonance imaging studies in bipolar disorder and schizophrenia: meta-analysis. British Journal of Psychiatry 195, 194–201.CrossRefGoogle ScholarPubMed
Arts, B, Jabben, N, Krabbendam, L, Van Os, J (2008). Meta-analyses of cognitive functioning in euthymic bipolar patients and their first-degree relatives. Psychological Medicine 38, 771–785.CrossRefGoogle ScholarPubMed
Barnett, JH, Salmond, CH, Jones, PB, Sahakian, BJ (2006). Cognitive reserve in neuropsychiatry. Psychological Medicine 36, 1053–1064.CrossRefGoogle ScholarPubMed
Basso, MR, Bornstein, RA (2000). Estimated premorbid intelligence mediates neurobehavioral change in individuals infected with HIV across 12 months. Journal of Clinical and Experimental Neuropsychology 22, 208–218.CrossRefGoogle Scholar
Benjamini, Y, Hochberg, Y (1995). Controlling the false discovery rate – a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57, 289–300.Google Scholar
Bourne, C, Aydemir, O, Balanza-Martinez, V, Bora, E, Brissos, S, Cavanagh, JT, Clark, L, Cubukcuoglu, Z, Dias, VV, Dittmann, S, Ferrier, IN, Fleck, DE, Frangou, S, Gallagher, P, Jones, L, Kieseppa, T, Martinez-Aran, A, Melle, I, Moore, PB, Mur, M, Pfennig, A, Raust, A, Senturk, V, Simonsen, C, Smith, DJ, Bio, DS, Soeiro-De-Souza, MG, Stoddart, SD, Sundet, K, Szoke, A, Thompson, JM, Torrent, C, Zalla, T, Craddock, N, Andreassen, OA, Leboyer, M, Vieta, E, Bauer, M, Worhunsky, PD, Tzagarakis, C, Rogers, RD, Geddes, JR, Goodwin, GM (2013). Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: an individual patient data meta-analysis. Acta Psychiatrica Scandinavica 128, 149–162.CrossRefGoogle ScholarPubMed
Boyle, PA, Wilson, RS, Schneider, JA, Bienias, JL, Bennett, DA (2008). Processing resources reduce the effect of Alzheimer pathology on other cognitive systems. Neurology 70, 1534–1542.CrossRefGoogle ScholarPubMed
Brickman, AM, Siedlecki, KL, Muraskin, J, Manly, JJ, Luchsinger, JA, Yeung, LK, Brown, TR, Decarli, C, Stern, Y (2011). White matter hyperintensities and cognition: testing the reserve hypothesis. Neurobiology of Aging 32, 1588–1598.CrossRefGoogle ScholarPubMed
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179–194.CrossRefGoogle ScholarPubMed
Deary, IJ, Leaper, SA, Murray, AD, Staff, RT, Whalley, LJ (2003). Cerebral white matter abnormalities and lifetime cognitive change: a 67-year follow-up of the Scottish Mental Survey of 1932. Psychology and Aging 18, 140–148.CrossRefGoogle Scholar
Desikan, RS, Segonne, F, Fischl, B, Quinn, BT, Dickerson, BC, Blacker, D, Buckner, RL, Dale, AM, Maguire, RP, Hyman, BT, Albert, MS, Killiany, RJ (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31, 968–980.CrossRefGoogle ScholarPubMed
Dufouil, C, Alperovitch, A, Tzourio, C (2003). Influence of education on the relationship between white matter lesions and cognition. Neurology 60, 831–836.CrossRefGoogle ScholarPubMed
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences USA 97, 11050–11055.CrossRefGoogle ScholarPubMed
Fischl, B, Salat, DH, Busa, E, Albert, M, Dieterich, M, Haselgrove, C, Van Der Kouwe, A, Killiany, R, Kennedy, D, Klaveness, S, Montillo, A, Makris, N, Rosen, B, Dale, AM (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341–355.CrossRefGoogle ScholarPubMed
Fischl, B, Salat, DH, Van Der Kouwe, AJ, Makris, N, Segonne, F, Quinn, BT, Dale, AM (2004 a). Sequence-independent segmentation of magnetic resonance images. NeuroImage 23 (Suppl. 1), S69–S84.CrossRefGoogle ScholarPubMed
Fischl, B, Sereno, MI, Dale, AM (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9, 195–207.CrossRefGoogle Scholar
Fischl, B, Van Der Kouwe, A, Destrieux, C, Halgren, E, Segonne, F, Salat, DH, Busa, E, Seidman, LJ, Goldstein, J, Kennedy, D, Caviness, V, Makris, N, Rosen, B, Dale, AM (2004 b). Automatically parcellating the human cerebral cortex. Cerebral Cortex 14, 11–22.CrossRefGoogle ScholarPubMed
Forcada, I, Mur, M, Mora, E, Vieta, E, Bartres-Faz, D, Portella, MJ (2015). The influence of cognitive reserve on psychosocial and neuropsychological functioning in bipolar disorder. European Neuropsychopharmacology 25, 214–222.CrossRefGoogle ScholarPubMed
Galioto, RM, Alosco, ML, Spitznagel, MB, Stanek, KM, Gunstad, J (2013). Cognitive reserve preserves cognitive function in obese individuals. Neuropsychology, Development, and Cognition. Section B: Aging, Neuropsychology and Cognition 20, 684–699.CrossRefGoogle ScholarPubMed
Gunde, E, Blagdon, R, Hajek, T (2011). White matter hyperintensities: from medical comorbidities to bipolar disorders and back. Annals of Medicine 43, 571–580.CrossRefGoogle ScholarPubMed
Guy, W (1976). Clinical Global Impression Scale. In ECDEU Assessment Manual for Psychopharmacology, revised (ed. Guy, W.), pp. 218–222. US Department of Health, Education, and Welfare, Public Health Service, Alcohol, Drug Abuse, and Mental Health Administration, National Institute of Mental Health, Psychopharmacology Research Branch, Division of Extramural Research Programs: Rockville, MD.Google Scholar
Harrison, SL, Sajjad, A, Bramer, WM, Ikram, MA, Tiemeier, H, Stephan, BC (2015). Exploring strategies to operationalize cognitive reserve: a systematic review of reviews. Journal of Clinical and Experimental Neuropsychology 37, 253–264.CrossRefGoogle ScholarPubMed
Iltis, AS, Misra, S, Dunn, LB, Brown, GK, Campbell, A, Earll, SA, Glowinski, A, Hadley, WB, Pies, R, Dubois, JM (2013). Addressing risks to advance mental health research. JAMA Psychiatry 70, 1363–1371.CrossRefGoogle ScholarPubMed
Jack, CR Jr., Twomey, CK, Zinsmeister, AR, Sharbrough, FW, Petersen, RC, Cascino, GD (1989). Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 172, 549–554.CrossRefGoogle ScholarPubMed
Karp, A, Kareholt, I, Qiu, C, Bellander, T, Winblad, B, Fratiglioni, L (2004). Relation of education and occupation-based socioeconomic status to incident Alzheimer's disease. American Journal of Epidemiology 159, 175–183.CrossRefGoogle ScholarPubMed
Kempton, MJ, Geddes, JR, Ettinger, U, Williams, SC, Grasby, PM (2008). Meta-analysis, database, and meta-regression of 98 structural imaging studies in bipolar disorder. Archives of General Psychiatry 65, 1017–1032.CrossRefGoogle ScholarPubMed
Kesner, RP, Churchwell, JC (2011). An analysis of rat prefrontal cortex in mediating executive function. Neurobiology of Learning and Memory 96, 417–431.CrossRefGoogle ScholarPubMed
Kontis, D, Huddy, V, Reeder, C, Landau, S, Wykes, T (2013). Effects of age and cognitive reserve on cognitive remediation therapy outcome in patients with schizophrenia. American Journal of Geriatric Psychiatry 21, 218–230.CrossRefGoogle ScholarPubMed
Lazarov, O, Robinson, J, Tang, YP, Hairston, IS, Korade-Mirnics, Z, Lee, VM, Hersh, LB, Sapolsky, RM, Mirnics, K, Sisodia, SS (2005). Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell 120, 701–713.CrossRefGoogle ScholarPubMed
Lezak, M, Howieson, D, Bigler, E, Tranel, D (2012). Neuropsychological Assessment. Oxford University Press: New York.Google Scholar
Lopez-Larson, MP, Delbello, MP, Zimmerman, ME, Schwiers, ML, Strakowski, SM (2002). Regional prefrontal gray and white matter abnormalities in bipolar disorder. Biological Psychiatry 52, 93–100.CrossRefGoogle ScholarPubMed
Luders, E, Narr, KL, Thompson, PM, Rex, DE, Woods, RP, Deluca, H, Jancke, L, Toga, AW (2006). Gender effects on cortical thickness and the influence of scaling. Human Brain Mapping 27, 314–324.CrossRefGoogle ScholarPubMed
Maller, JJ, Thaveenthiran, P, Thomson, RH, McQueen, S, Fitzgerald, PB (2014). Volumetric, cortical thickness and white matter integrity alterations in bipolar disorder type I and II. Journal of Affective Disorders 169, 118–127.CrossRefGoogle ScholarPubMed
Miller, EK, Cohen, JD (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24, 167–202.CrossRefGoogle ScholarPubMed
Mortimer, JA, Borenstein, AR, Gosche, KM, Snowdon, DA (2005). Very early detection of Alzheimer neuropathology and the role of brain reserve in modifying its clinical expression. Journal of Geriatric Psychiatry and Neurology 18, 218–223.CrossRefGoogle ScholarPubMed
Mortimer, JA, Snowdon, DA, Markesbery, WR (2003). Head circumference, education and risk of dementia: findings from the Nun Study. Journal of Clinical and Experimental Neuropsychology 25, 671–679.CrossRefGoogle ScholarPubMed
Oertel-Knochel, V, Reinke, B, Alves, G, Jurcoane, A, Wenzler, S, Prvulovic, D, Linden, D, Knochel, C (2014). Frontal white matter alterations are associated with executive cognitive function in euthymic bipolar patients. Journal of Affective Disorders 155, 223–233.CrossRefGoogle ScholarPubMed
Olsson, E, Klasson, N, Berge, J, Eckerstrom, C, Edman, A, Malmgren, H, Wallin, A (2013). White matter lesion assessment in patients with cognitive impairment and healthy controls: reliability comparisons between visual rating, a manual, and an automatic volumetrical MRI method – the Gothenburg MCI study. Journal of Aging Research 2013, 198471.Google Scholar
Ovbiagele, B, Saver, JL (2006). Cerebral white matter hyperintensities on MRI: current concepts and therapeutic implications. Cerebrovascular Diseases 22, 83–90.CrossRefGoogle ScholarPubMed
Palsson, E, Figueras, C, Johansson, AG, Ekman, CJ, Hultman, B, Ostlind, J, Landen, M (2013). Neurocognitive function in bipolar disorder: a comparison between bipolar I and II disorder and matched controls. BMC Psychiatry 13, 165.CrossRefGoogle ScholarPubMed
Pereda, M, Ayuso-Mateos, JL, Gomez Del Barrio, A, Echevarria, S, Farinas, MC, Garcia Palomo, D, Gonzalez Macias, J, Vazquez-Barquero, JL (2000). Factors associated with neuropsychological performance in HIV-seropositive subjects without AIDS. Psychological Medicine 30, 205–217.CrossRefGoogle ScholarPubMed
Perlis, RH, Dennehy, EB, Miklowitz, DJ, Delbello, MP, Ostacher, M, Calabrese, JR, Ametrano, RM, Wisniewski, SR, Bowden, CL, Thase, ME, Nierenberg, AA, Sachs, G (2009). Retrospective age at onset of bipolar disorder and outcome during two-year follow-up: results from the STEP-BD study. Bipolar Disorders 11, 391–400.CrossRefGoogle ScholarPubMed
Poletti, S, Bollettini, I, Mazza, E, Locatelli, C, Radaelli, D, Vai, B, Smeraldi, E, Colombo, C, Benedetti, F (2015). Cognitive performances associate with measures of white matter integrity in bipolar disorder. Journal of Affective Disorders 174, 342–352.CrossRefGoogle ScholarPubMed
Post, RM, Leverich, GS, Kupka, RW, Keck, PE Jr., McElroy, SL, Altshuler, LL, Frye, MA, Luckenbaugh, DA, Rowe, M, Grunze, H, Suppes, T, Nolen, WA (2010). Early-onset bipolar disorder and treatment delay are risk factors for poor outcome in adulthood. Journal of Clinical Psychiatry 71, 864–872.CrossRefGoogle ScholarPubMed
Quinn, NP, Rossor, MN, Marsden, CD (1986). Dementia and Parkinson's disease – pathological and neurochemical considerations. British Medical Bulletin 42, 86–90.CrossRefGoogle ScholarPubMed
Rentz, DM, Huh, TJ, Faust, RR, Budson, AE, Scinto, LF, Sperling, RA, Daffner, KR (2004). Use of IQ-adjusted norms to predict progressive cognitive decline in highly intelligent older individuals. Neuropsychology 18, 38–49.CrossRefGoogle ScholarPubMed
Rimol, LM, Nesvag, R, Hagler, DJ Jr., Bergmann, O, Fennema-Notestine, C, Hartberg, CB, Haukvik, UK, Lange, E, Pung, CJ, Server, A, Melle, I, Andreassen, OA, Agartz, I, Dale, AM (2012). Cortical volume, surface area, and thickness in schizophrenia and bipolar disorder. Biological Psychiatry 71, 552–560.CrossRefGoogle ScholarPubMed
Ryden, E, Thase, ME, Straht, D, Aberg-Wistedt, A, Bejerot, S, Landen, M (2009). A history of childhood attention-deficit hyperactivity disorder (ADHD) impacts clinical outcome in adult bipolar patients regardless of current ADHD. Acta Psychiatrica Scandinavica 120, 239–246.CrossRefGoogle ScholarPubMed
Sachs, GS, Thase, ME, Otto, MW, Bauer, M, Miklowitz, D, Wisniewski, SR, Lavori, P, Lebowitz, B, Rudorfer, M, Frank, E, Nierenberg, AA, Fava, M, Bowden, C, Ketter, T, Marangell, L, Calabrese, J, Kupfer, D, Rosenbaum, JF (2003). Rationale, design, and methods of the systematic treatment enhancement program for bipolar disorder (STEP-BD). Biological Psychiatry 53, 1028–1042.CrossRefGoogle ScholarPubMed
Satz, P (1993). Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology 7, 273–295.CrossRefGoogle Scholar
Sax, KW, Strakowski, SM, Zimmerman, ME, Delbello, MP, Keck, PE Jr., Hawkins, JM (1999). Frontosubcortical neuroanatomy and the continuous performance test in mania. American Journal of Psychiatry 156, 139–141.CrossRefGoogle ScholarPubMed
Schmand, B, Smit, JH, Geerlings, MI, Lindeboom, J (1997). The effects of intelligence and education on the development of dementia. A test of the brain reserve hypothesis. Psychological Medicine 27, 1337–1344.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59 (Suppl. 20), 22–33.Google ScholarPubMed
Sparding, T, Silander, K, Palsson, E, Ostlind, J, Sellgren, C, Ekman, CJ, Joas, E, Hansen, S, Landen, M (2015). Cognitive functioning in clinically stable patients with bipolar disorder I and II. PLOS ONE 10, e0115562.CrossRefGoogle ScholarPubMed
Spreen, O, Strauss, E (1991). A Compendium of Neuropsychological Tests: Administration, Norms, and Commentary. Oxford University Press: New York.Google Scholar
Steffener, J, Reuben, A, Rakitin, BC, Stern, Y (2011). Supporting performance in the face of age-related neural changes: testing mechanistic roles of cognitive reserve. Brain Imaging and Behavior 5, 212–221.CrossRefGoogle ScholarPubMed
Stern, RA, Silva, SG, Chaisson, N, Evans, DL (1996). Influence of cognitive reserve on neuropsychological functioning in asymptomatic human immunodeficiency virus-1 infection. Archives of Neurology 53, 148–153.CrossRefGoogle ScholarPubMed
Stern, Y (2002). What is cognitive reserve? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society 8, 448–460.CrossRefGoogle ScholarPubMed
Stern, Y (2009). Cognitive reserve. Neuropsychologia 47, 2015–2028.CrossRefGoogle ScholarPubMed
Stern, Y (2012). Cognitive reserve in ageing and Alzheimer's disease. Lancet Neurology 11, 1006–1012.CrossRefGoogle ScholarPubMed
Stern, Y, Zarahn, E, Habeck, C, Holtzer, R, Rakitin, BC, Kumar, A, Flynn, J, Steffener, J, Brown, T (2008). A common neural network for cognitive reserve in verbal and object working memory in young but not old. Cerebral Cortex 18, 959–967.CrossRefGoogle Scholar
Stern, Y, Zarahn, E, Hilton, HJ, Flynn, J, Delapaz, R, Rakitin, B (2003). Exploring the neural basis of cognitive reserve. Journal of Clinical and Experimental Neuropsychology 25, 691–701.CrossRefGoogle ScholarPubMed
Strakowski, SM, Delbello, MP, Adler, CM (2005). The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Molecular Psychiatry 10, 105–16.CrossRefGoogle ScholarPubMed
Sumowski, JF, Chiaravalloti, N, Wylie, G, Deluca, J (2009). Cognitive reserve moderates the negative effect of brain atrophy on cognitive efficiency in multiple sclerosis. Journal of the International Neuropsychological Society 15, 606–612.CrossRefGoogle ScholarPubMed
Torres, IJ, Boudreau, VG, Yatham, LN (2007). Neuropsychological functioning in euthymic bipolar disorder: a meta-analysis. Acta Psychiatrica Scandinavica Supplementum 116 (Suppl. s434), 17–26.CrossRefGoogle Scholar
Valenzuela, MJ, Sachdev, P (2006). Brain reserve and dementia: a systematic review. Psychological Medicine 36, 441–454.CrossRefGoogle ScholarPubMed
Van Praag, H, Shubert, T, Zhao, C, Gage, FH (2005). Exercise enhances learning and hippocampal neurogenesis in aged mice. Journal of Neuroscience 25, 8680–8685.CrossRefGoogle ScholarPubMed
Wechsler, D (1997). WAIS-III Administration and Scoring Manual. Psychological Corporation: San Antonio, TX.Google Scholar
Wolf, H, Julin, P, Gertz, HJ, Winblad, B, Wahlund, LO (2004). Intracranial volume in mild cognitive impairment, Alzheimer's disease and vascular dementia: evidence for brain reserve? International Journal of Geriatric Psychiatry 19, 995–1007.CrossRefGoogle ScholarPubMed
Yoshita, M, Fletcher, E, Decarli, C (2005). Current concepts of analysis of cerebral white matter hyperintensities on magnetic resonance imaging. Topics in Magnetic Resonance Imaging 16, 399–407.CrossRefGoogle ScholarPubMed