Skip to main content

Advertisement

Log in

Early dysfunction of functional connectivity in healthy elderly with subjective memory complaints

  • Published:
AGE Aims and scope Submit manuscript

A Correction to this article was published on 23 March 2022

This article has been updated

Abstract

It is still an open question whether subjective memory complaints (SMC) can actually be considered to be clinically relevant predictors for the development of an objective memory impairment and even dementia. There is growing evidence that suggests that SMC are associated with an increased risk of dementia and with the presence of biological correlates of early Alzheimer's disease. In this paper, in order to shed some light on this issue, we try to discern whether subjects with SMC showed a different profile of functional connectivity compared with subjects with mild cognitive impairment (MCI) and healthy elderly subjects. In the present study, we compare the degree of synchronization of brain signals recorded with magnetoencephalography between three groups of subjects (56 in total): 19 with MCI, 12 with SMC and 25 healthy controls during a memory task. Synchronization likelihood, an index based on the theory of nonlinear dynamical systems, was used to measure functional connectivity. Briefly, results show that subjects with SMC have a very similar pattern of connectivity to control group, but on average, they present a lower synchronization value. These results could indicate that SMC are representing an initial stage with a hypo-synchronization (in comparison with the control group) where the brain system is still not compensating for the failing memory networks, but behaving as controls when compared with the MCI subjects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Change history

References

  • Abdulrab K, Heun R (2008) Subjective memory impairment. A review of its definitions indicates the need for a comprehensive set of standardized and validated criteria. Eur Psychiatr 23:321–330

    Article  Google Scholar 

  • Bajo R, Maestú F, Nevado A, Sancho M et al (2010) Functional connectivity in mild cognitive impairment during a memory task: implications for the disconnection hypothesis. J Alzheimers Dis 22:183–193

    PubMed  Google Scholar 

  • Bassett SS, Folstein (1993) MF: memory complaint, memory performance performance, and psychiatric diagnosis: a community study. J Geriatr Psychiatr Neurol 6:105–111

    CAS  Google Scholar 

  • Benito-León J, Mitchell AJ, Vega S, Bermejo-Pareja F (2010) A population-based study of cognitive function in older people with subjective memory complaints. J Alzheimers Dis 22(1):159–170

    PubMed  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29(4):1165–1188

    Article  Google Scholar 

  • Bolla KI, Lindgren KN, Bonaccorsy C, Bleecker ML (1991) Memory complaints in older adults. Arch Neurol 48:61–64

    Article  PubMed  CAS  Google Scholar 

  • Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259

    Article  PubMed  CAS  Google Scholar 

  • deToledo-Morrell L, Evers S, Hoeppner TJ, Morrell F, Garron DC, Fox JH (1991) A ‘stress’ test for memory dysfunction. Electrophysiologic manifestations of early Alzheimer's disease. Arch Neurol 48:605–609

    Article  PubMed  CAS  Google Scholar 

  • Cabeza R, Dolcos F, Graham R, Nyberg L (2002) Similarities and differences in the neural correlates of episodic memory retrieval and working memory. Neuroimage 16:317–330

    Article  PubMed  Google Scholar 

  • Elfgren C, Gustafson L, Vestberg S, Passant U (2010) Subjective memory complaints, neuropsychological performance and psychiatric variables in memory clinic attendees: a 3-year follow-up study. Arch Gerontol Geriatr 51(3):e110–e114

    Article  PubMed  Google Scholar 

  • Farias ST, Mungas D, Jagust W (2005) Degree of discrepancy between self and other- reported everyday functioning by cognitive status: dementia, mild cognitive impairment and healthy elders. Int J Geriatr Psychiatry 20:827–834

    Article  PubMed  Google Scholar 

  • Gagnon M, Dartigues JF, Mazaux JM, Dequae L, Letenneur L, Giroire JM, Barberger-Gateau P (1994) Self-reported memory complaints and memory performance in elderly French community residents: results of the PAQUID research program. Neuroepidemiology 13(4):145–154

    Article  PubMed  CAS  Google Scholar 

  • Gallassi R, Oppi F, Poda R, Scortichini S, Stanzani Maserati M, Marano G, Sambati L (2010) Are subjective cognitive complaints a risk factor for dementia? Neurol Sci 31(3):327–336

    Article  PubMed  Google Scholar 

  • Ganguli M, Dodge HH, Shen C, DeKosky ST (2004) Mild cognitive impairment, amnestic type: an epidemiologic study. Neurology 63:115–121

    PubMed  Google Scholar 

  • Genovese R, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878

    Article  PubMed  Google Scholar 

  • Glodzik-Sobanska L, Reisberg B, De Santi S, Babb JS, Pirraglia E, Rich KE, Brys M, de Leon MJ (2007) Subjective memory complaints: presence, severity and future outcome in normal older subjects. Dement Geriatr Cogn Disord 24:177–184.

    Article  PubMed  Google Scholar 

  • Grundman M, Petersen RC, Ferris SH, Thomas RG, Aisen PS, Bennett DA et al (2004) Mild cognitive impairment can be distinguished from Alzheimer disease and normal aging for clinical trials. Arch Neurol 61:59–66

    Article  PubMed  Google Scholar 

  • Guggisberg AG, Honma SM, Findlay A, Dalal SS, Kirsch HE, Berger MS et al (2008) Mapping functional connectivity in patients with brain lesions. Ann Neurol 63:193–203

    Article  PubMed  Google Scholar 

  • Jessen F, Feyen L, Freymann K, Tepest R, Maier W, Heun R et al (2006) Volume reduction of the entorhinal cortex in subjective memory impairment. Neurobiol Aging 27:1751–1756

    Article  PubMed  Google Scholar 

  • Jessen F, Wiese B, Cvetanovska G, Fuchs A, Kaduszkiewicz H, Kolsch H et al (2007) Patterns of subjective memory impairment in the elderly: association with memory performance. Psychol Med 37:1753–1762

    Article  PubMed  Google Scholar 

  • Jessen F, Wiese B, Bachmann C, Eifflaender-Gorfer S, Haller F, Kölsch H, Luck T, Mösch E, Van den Bussche H, Wagner M, Wollny A, Zimmermann T, Pentzek M, Riedel-Heller SG, Romberg HP, Weyerer S, Kaduszkiewicz H, Maier W, Bickel H (2010) Prediction of dementia by subjective memory impairment: effects of severity and temporal association with cognitive impairment. Arch Gen Psychiatr 67(4):414–422

    Article  PubMed  Google Scholar 

  • Jonker C, Launer LJ, Hooijer C, Lindeboom J (1996) Memory complaints and memory impairment in older individuals. J Am Geriatr Soc 44(1):44–49

    PubMed  CAS  Google Scholar 

  • Jonker C, Geerlings MI, Schmand B (2000) Are memory complaints predictive for dementia? A review of clinical and population- based studies. Int J Geriatr Psychiatry 15(11):983–991

    Article  PubMed  CAS  Google Scholar 

  • Jorm AF, Butterworth P, Anstey KJ et al (2004) Memory complaints in a community sample aged. 60–64 years: associations with cognitive functioning, psychiatric symptoms, medical conditions, APOE genotype, hippocampus and amygdala volumes, and white-matter hyperintensities. Psychol Med 34(8):1495–1506

    Article  PubMed  CAS  Google Scholar 

  • Lobo A, Ezquerra J, Gomez BF, Sala JM, Seva DA (1979) Cognocitive mini-test (a simple practical test to detect intellectual changes in medical patients). Actas Luso Esp Neurol Psiquiatr Cienc Afines 7:189–202

    PubMed  CAS  Google Scholar 

  • Luck T, Riedel-Heller SG, Luppa M, Wiese B, Wollny A, Wagner M, Bickel H, Weyerer S, Pentzek M, Haller F, Moesch E, Werle J, Eisele M, Maier W, Van Den Bussche H, Kaduszkiewicz H (2010) Risk factors for incident mild cognitive impairment—results from the German study on ageing, cognition and dementia in primary care patients (AgeCoDe). Acta Psychiatr Scand 121(4):260–272

    Article  PubMed  CAS  Google Scholar 

  • Maestu F, Fernandez A, Simos PG, Gil-Gregorio P, Amo C, Rodriguez R, Arrazola J, Ortiz T (2001) Spatio-temporal patterns of brain magnetic activity during a memory task in Alzheimer's disease. Neuroreport 12:3917–3922

    Article  PubMed  CAS  Google Scholar 

  • Maestu F, Baykova E, Ruiz JM, Montejo P, Montenegro M, Llanero M, Solesio E, Gil P, Yubero R, Paul N, Pozo F, Nevado A (2011) Increased biomagnetic activity in healthy elderly with subjective memory complaints. Clin Neurophysiol 122:499–505, Accepted

    Article  PubMed  Google Scholar 

  • Minett TSC, Da Silva RV, Ortiz KZ, Bertolucci PHF (2007) Subjective memory complaints in an elderly sample: a cross- sectional study. Int J Geriatr Psychiatry 23:49–54

    Article  Google Scholar 

  • Mitchell AJ (2008a) Is it time to separate subjective cognitive complaints from the diagnosis of mild cognitive impairment? Age Ageing 37:497–499

    Article  Google Scholar 

  • Mitchell AJ (2008b) The clinical significance of subjective memory complaints in the diagnosis of mild cognitive impairment and dementia: a meta-analysis. Int J Geriatr Psychiatry 23:1191–1202

    Article  Google Scholar 

  • Montez T, Linkenkaer-Hansen K, Van Dijk BW, Stam CJ (2006) Synchronization likelihood with explicit time-frequency priors. Neuroimage 33:1117–1125

    Article  PubMed  CAS  Google Scholar 

  • Morris R, Becker J (1994) Cognitive Neuropsychology of Alzheimer Disease. Oxford University Press

  • Mosconi L, De Santi S, Brys M, Tsui WH, Pirraglia E, Glodzik-Sobanska L et al (2008) Hypometabolism and altered cerebrospinal fluid markers in normal apolipoprotein E4 carriers with subjective memory complaints. Biol Psychiatr 63:609–618

    Article  CAS  Google Scholar 

  • Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256:183–194

    Article  PubMed  CAS  Google Scholar 

  • Riedel-Heller SG, Matschinger H (1999) Do memory complaints indicate the presence of cognitive impairment? Results of a field study. Eur Arch Psychiatr Neurol Sci 249:197–204

    Article  CAS  Google Scholar 

  • Roberts JL, Clare L, Woods RT (2009) Subjective memory complaints and awareness of memory functioning in mild cognitive impairment: a systematic review. Dement Geriatr Cognit Disord 28:95–109

    Article  CAS  Google Scholar 

  • Rodda JE, Dannhauser TM, Cutinha DJ, Shergill SS, Walker Z (2009) Subjective cognitive impairment: increased prefrontal cortex activation to control during an encoding task. Int J Geriatr Psychiatry 24:865–874

    Article  PubMed  Google Scholar 

  • Rodda J, Dannhauser T, Cutinha DJ, Shergill SS, Walker Z (2010) Subjective cognitive impairment: functional MRI during a divided attention task. Eur Psychiatr. doi:10.1016/j.eurpsy.2010.07.003, ISSN 0924–9338

    Google Scholar 

  • Schmand B, Jonker C, Hooijer C, Lindeboom J (1996) Subjective memory complaints may announce dementia. Neurology 46(1):121–125

    PubMed  CAS  Google Scholar 

  • Schnitzler A, Gross J (2005) Normal and pathological oscillatory communication in the brain. Nat Rev Neurosci 6:285–296

    Article  PubMed  CAS  Google Scholar 

  • Stam CJ, Van Dijk BW (2002) Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets. Physica D 163:236–241

    Article  Google Scholar 

  • Stam CJ, De Haan W, Daffertshofer A, Jones BF, Manshanden I, Van Cappellen van Walsum AM et al (2009) Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. Brain 132:213–224

    Article  PubMed  CAS  Google Scholar 

  • Stenset V, Hofoss D, Berstad AE, Negaard A, Gjerstad L, Fladby T (2008) White matter lesion subtypes and cognitive deficits in patients with memory impairment. Dement Geriatr Cognit Disord 26:424–431

    Article  Google Scholar 

  • Sunderland A, Harris JE, Baddeley AD (1983) Do laboratory tests predict everyday memory? A neuropsychological study. Journal of Verbal Learning and Verbal Behavior 22(3):341–357. doi:10.1016/S0022-5371(83)90229-3, ISSN 0022–5371

    Article  Google Scholar 

  • Tobiansky R, Blizard R, Livingston G, Mann A (1995) The gospel oak study stage IV: the clinical relevance of subjective memory impairment in older people. Psychol Med 25:779–786

    Article  PubMed  CAS  Google Scholar 

  • Treves TA, Verchovsky R, Klimovitzky S, Korczyn AD (2005) Incidence of dementia in patients with subjective memory complaints. Int Psychogeriatr 17:265–273.

    Article  PubMed  CAS  Google Scholar 

  • Van der Flier WM, Van Buchem MA, Weverling-Rijnsburger AW, Mutsaers ER, Bollen EL, Admiraal-Behloul F et al (2004) Memory complaints in patients with normal cognition are associated with smaller hippocampal volumes. J Neurol 251(6):671–675

    Article  PubMed  Google Scholar 

  • Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229–239

    Article  PubMed  CAS  Google Scholar 

  • Vestberg S, Passant U, Elfgren C (2010) Stability in the clinical characteristics of patients with memory complaints. Arch Gerontol Geriatr 50:e26–e30

    Article  PubMed  Google Scholar 

  • Wang L, Van Belle G, Crane PK, Kukull WA, Bowen JD, McCormick WC, Larson EB (2004) Subjective memory deterioration and future dementia in people aged 65 and older. J Am Geriatr Soc 52:2045–2051.

    Article  PubMed  Google Scholar 

  • Yesavage JA, Brooks JO (1991) On the importance of longitudinal research in Alzheimer's disease. J Am Geriatr Soc 39(9):942–944

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by two grants for the Spanish Ministry of Science and Innovation (SEJ-2006-07560; PSI2009-14415-C03-01).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ricardo Bajo.

About this article

Cite this article

Bajo, R., Castellanos, N.P., López, M.E. et al. Early dysfunction of functional connectivity in healthy elderly with subjective memory complaints. AGE 34, 497–506 (2012). https://doi.org/10.1007/s11357-011-9241-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-011-9241-5

Keywords

Navigation