Skip to main content

Advertisement

Log in

Word-stem priming and recognition in type 2 diabetes mellitus, Alzheimer’s disease patients and healthy older adults

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The present study investigated (a) whether the pattern of performance on implicit and explicit memory of patients with type 2 diabetes mellitus (DM2) is more similar to those of patients with Alzheimer’s disease (AD) or to cognitively normal older adults and (b) whether glycosylated hemoglobin levels (a measure of glucose regulation) are related to performance on the two memory tasks, implicit word-stem completion and “old–new” recognition. The procedures of both memory tasks included encoding and memory test phases separated by a short delay. Three groups of participants (healthy older adults, DM2 patients and AD patients) completed medical and psychological assessments and performed both memory tasks on a computer. The results of the word-stem completion task showed similar implicit memory in the three groups. By contrast, explicit recognition of the three groups differed. Implicit memory was not affected by either normal or pathological aging, but explicit memory deteriorated in the two groups of patients, especially in AD patients, showing a severe impairment compared to the cognitively healthy older adults. Importantly, glycosylated hemoglobin levels were not related to performance on either implicit or explicit memory tasks. These findings revealed a clear dissociation between explicit and implicit memory tasks in normal and pathological aging. Neuropsychologists and clinicians working with TM2 patients should be aware that the decline of voluntary, long-term explicit memory could have a negative impact on their treatment management. By contrast, the intact implicit memory of the two clinical groups could be used in rehabilitation.

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

Similar content being viewed by others

References

  • Alameda JR, Cuetos F (1995) Diccionario de frecuencias de las unidades lingüísticas del castellano. In: Oviedo U (ed) vol I, II. Oviedo, Servicio de publicaciones de la universidad de Oviedo

  • Asimakopoulou KG, Hampson SE, Morrish NJ (2002) Neuropsychological functioning in older people with type 2 diabetes: the effect of controlling for confounding factors. Diabet Med 19:311–316

    Article  CAS  PubMed  Google Scholar 

  • Awad N, Gagnon M, Messier C (2004) The relationship between impaired glucose tolerance, type 2 diabetes and cognitive function. Exp Neuropsychol 26:1044–1080

    Article  Google Scholar 

  • Ballesteros S, Reales JM (2004) Intact haptic priming in normal aging and Alzheimer’s disease: evidence for dissociable memory systems. Neuropsychologia 44:1063–1070

    Article  Google Scholar 

  • Ballesteros S, Reales JM, Mayas J, Heller MA (2008) Selective attention modulates visual and haptic repetition priming: effects in aging and Alzheimer’s disease. Exp Brain Res 189:473–483. doi:10.1007/s00221-008-1441-6

    Article  PubMed  Google Scholar 

  • Ballesteros S, González M, Mayas J, García-Rodríguez B, Reales JM (2009) Cross-modal repetition priming in young and old adults. Eur J Cogn Psychol 21:366–387

    Article  Google Scholar 

  • Ballesteros S, Bischof GN, Goh JO, Park DC (2013a) Neural correlates of conceptual object priming in young and older adults: an event-related functional magnetic resonance imaging study. Neurobiol Aging 34:1254–1264. doi:10.1016/j.neurobiolaging.2012.09.019

    Article  PubMed Central  PubMed  Google Scholar 

  • Ballesteros S, Mayas J, Reales JM (2013b) Cognitive function in normal aging and in older adults with mild cognitive impairment. Psicothema 25:18–24

    PubMed  Google Scholar 

  • Barbagallo M, Dominguez LJ (2014) Type 2 diabetes mellitus and Alzheimer’s disease. World J Diabetes 5:889–893. doi:10.4239/wjd.v5.i6.889

    Article  PubMed Central  PubMed  Google Scholar 

  • Bauduceau B, Doucet J, Bordier L, Garcia C, Dupuy O, Mayaudon H (2010) Hypoglycaemia and dementia in diabetic patients. Diabetes Metab 36:S106–S111

    Article  CAS  PubMed  Google Scholar 

  • Bondi MW, Kaszniak AW (1991) Implicit and explicit memory in Alzheimer’s disease and Parkinson’s disease. J Clin Exp Neuropsychol 13:339–358. doi:10.1080/01688639108401048

    Article  CAS  PubMed  Google Scholar 

  • Bosco D, Fava A, Plastino M, Montalcini T, Pujia A (2011) Possible implications of insulin resistance and glucose metabolism in Alzheimer’s disease pathogenesis. J Cell Mol Med 15:1807–1821. doi:10.1111/j.1582-4934.2011.01318.x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brookmeyer R, Evans DA, Hebert L, Langa KM, Heeringa SG, Plassman BL, Kukull WA (2011) National estimates of the prevalence of Alzheimer’s disease in the United States. Alzheimers Dement 7:61–73. doi:10.1016/j.jalz.2010.11.007

    Article  PubMed Central  PubMed  Google Scholar 

  • Bruehl H, Rueger M, Dziobek I, Sweat V, Tirsi A, Javier E, Arentoft A, Wolf OT, Convit A (2007) Hypothalamic-pituitary-adrenal axis dysregulation and memory impairments in type 2 diabetes. J Clin Endocrinol Metab 92:2439–2445. doi:10.1210/jc.2006-2540

    Article  CAS  PubMed  Google Scholar 

  • Brun A, Englund E (1981) Regional pattern of degeneration in Alzheimer’s disease: neuronal loss and histopathological grading. Histopathology 5:549–564. doi:10.1111/j.1365-2559.1981.tb01818.x

    Article  CAS  PubMed  Google Scholar 

  • Cervantes-Arriaga A, Rodriguez-Violante M, Calleja-Castillo J, Ramirez-Bermudez J (2011) Función cognitiva en pacientes con diabetes mellitus tipo 2: correlación metabólica y por imagen de resonancia magnética. Med Int Mex 27:217–223

    Google Scholar 

  • CIBERDEM (2010) Prevalencia de la diabetes en España: Estudio di@bet.es. Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas

  • Convit A (2005) Links between cognitive impairment in insulin resistance: an explanatory model. Neurobiol Aging S26:S31–S35. doi:10.1016/j.neurobiolaging.2005.09.018

    Article  Google Scholar 

  • Craft S (2005) Insulin resistance syndrome and Alzheimer’s disease: age-and obesity-related effects on memory, amyloid, and inflammation. Neurobiol Aging 26S:S65–S69

    Article  Google Scholar 

  • Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ et al (2011) National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378:31–40

    Article  CAS  PubMed  Google Scholar 

  • Fay S, Pouthas V, Ragot R, Isingrini M (2005) Neural correlates of word-stem priming. Neuroreport 16:1169–1173

    Article  PubMed  Google Scholar 

  • Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, Hall K, Scafuzca M (2006) Global prevalence of dementia: a Delphi consensus study. Lancet 366:2112–2117. doi:10.1016/S0140-6736(05)67889-0

    Article  Google Scholar 

  • Fleischman DA (2007) Repetition priming in aging and Alzheimer’s disease: an integrative review and future directions. Cortex 43:889–897. doi:10.1016/S0010-9452(08)70688-9

    Article  PubMed  Google Scholar 

  • Fleischman DA, Gabrieli JDE (1998) Repetition priming in normal aging and Alzheimer’s disease: a review of findings and theories. Psychol Aging 13:88–119

    Article  CAS  PubMed  Google Scholar 

  • Fleischman DA, Vaidya CJ, Lange KL, Gabrieli JDE (1997) A dissociation between perceptual explicit and implicit memory processes. Brain Cogn 35:42–57

    Article  CAS  PubMed  Google Scholar 

  • Fleischman DA, Monti LA, Dwornik LM, Moro TT, Bennett DA, Gabrieli JDE (2001) Impaired production priming and intact identification priming in Alzheimer’s disease. J Int Neuropsychol Soc 7:785–794

    CAS  PubMed  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  • Gabrieli JD, Keane MM, Stanger BZ, Kjelgaard MM, Corkin S, Growdon JH (1994) Dissociations among structural–perceptual, lexical–semantic, and event–fact memory systems in Alzheimer, amnesic, and normal subjects. Cortex 30:75–103. doi:10.1016/S0010-9452(13)80325-5

    Article  CAS  PubMed  Google Scholar 

  • Gabrieli JD, Vaidya CJ, Stone M (1999) Convergent behavioral and neuropsychological evidence for a distinction between identification and production forms of repetition priming. J Exp Psychol Gen 128:479–498

    Article  CAS  PubMed  Google Scholar 

  • Gordon LT, Soldan A, Thomas AK, Stern Y (2013) Effects of repetition lag on priming of unfamiliar visual objects in young and older adults. Psychol Aging 28:219–231

    Article  PubMed Central  PubMed  Google Scholar 

  • Han W, Li C (2010) linking type 2 diabetes and Alzheimer’s disease. PNAS 107:6557–6558. doi:10.1073/pnas.1002555107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hoyer WJ, Verhaeghen P (2006) Memory aging. Elsevier, USA

    Google Scholar 

  • Huang J, Schmeidler J, Beeri MS, Rosendorff C, Bhatia S, West RK, Bespalova IN, Mavris R, Silverman JM (2012) Haemoglobin A1c and cognitive function in very old, cognitively intact men. Age Ageing 41:125–128. doi:10.1093/ageing/afr124

    Article  PubMed Central  PubMed  Google Scholar 

  • Karlsson T, Adolfsson R, Borjesson A, Nilsson LG (2003) Primed word-fragment completion and successive memory test performance in normal aging. Scand J Psychol 44:355–361

    Article  PubMed  Google Scholar 

  • Kuljis R, Salkovic-Petrisic M (2011) Dementia, diabetes, Alzheimer’s disease, and insulin resistance in the brain: progress, dilemmas, new opportunities, and a hypothesis to tackle intersecting epidemics. J Alzheimers Dis 25:29–41. doi:10.3233/JAD-2011-101392

    CAS  PubMed  Google Scholar 

  • La Voie D, Light LL (1994) Adult age differences in repetition priming: a meta-analysis. Psychol Aging 4:538–553. doi:10.1037/0882-7974.9.4.539

    Google Scholar 

  • Liu Y, Liu F, Grundke-Iqbal I, Iqbal K, Gong C (2009) Brain glucose transporters, O-GlcNAcylation and phosphorylation of tau in diabetes and Alzheimer disease. J Neurochem 111:242–249. doi:10.1111/j.1471-4159.2009.06320.x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Luchsinger JA (2012) Type 2 diabetes and cognitive impairment: linking mechanisms. J Alzheimers Dis 30:185–198. doi:10.3233/JAD-2012-111433

    Google Scholar 

  • Masdeu J (2004) Neuroimaging in Alzheimer’s disease: an overview. Rev Neurol 38:1156–1165

    CAS  PubMed  Google Scholar 

  • Matsuzaki T, Sasaki K, Tanizaki Y, Hata J, Fujimi K et al (2010) Insulin resistance is associated with the pathology of Alzheimer disease: the Hisayama study. Neurology 75:764–770. doi:10.1212/WNL.0b013e3181eee25f

    Article  CAS  PubMed  Google Scholar 

  • McCrimmon RJ, Ryan CM, Frier BM (2012) Diabetes and cognitive disfunction. Lancet 379:2291–2300. doi:10.1016/SO140-6736(12)60360-2

    Article  PubMed  Google Scholar 

  • McKhann G, Drachman D, Folstein MF et al (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group. Neurology 34:939–944

    Article  CAS  PubMed  Google Scholar 

  • Meier B, Graf P (2000) Transfer appropriate processing for prospective memory tests. Appl Cogn Psychol 14:S11–S27. doi:10.1002/acp.768

    Article  Google Scholar 

  • Messier C, Tsiakas M, Gagnon C, Desrochers A (2010) Effect of age and glucoregulation on cognitive performance. J Clin Exp Neuropsychol 32:809–821. doi:10.1080/13803390903540323

    Article  PubMed  Google Scholar 

  • Meusel LC, Kansal N, Tchistiakova E, Yuen W, MacIntosh BJ et al (2014) A systematic review of type 2 diabetes mellitus and hypertension in imaging studies of cognitive aging: time to establish new norms. Front Aging Neurosci 6:1–17. doi:10.3389/fnagi.2014.00148

    Article  Google Scholar 

  • Mitchell DB (1989) How many memory systems? Evidence from ageing. J Exp Psychol Learn 15:31–49

    Article  CAS  Google Scholar 

  • Mitchell DB, Bruss PJ (2003) Age differences in implicit memory: conceptual, perceptual, or methodological? Psychol Aging 18:807–822. doi:10.1037/0882-7974.18.4.807

    Article  PubMed  Google Scholar 

  • Monette MC, Baird A, Jackson DL (2014) A meta-analysis of cognitive functioning in nondemented adults with type 2 diabetes mellitus. Can J Diabetes 38:401–408. doi:10.1016/j.jcjd.2014.01.014

    Article  PubMed  Google Scholar 

  • Morris CD, Bransford JD, Franks JJ (1977) Levels of processing versus transfer appropriate processing. J Verbal Learning Verbal Behav 16:519–533. doi:10.1016/S0022-5371(77)80016-9

    Article  Google Scholar 

  • Nilson LG (2003) Memory function in normal aging. Acta Neurol Scand 107:7–13

    Article  Google Scholar 

  • Nilsson E, Whalin A (2009) Diabetes and elevated glycosylated hemoglobin: episodic memory and utilization of cognitive support. Eur J Cogn Psychol 21:388–405. doi:10.1080/09541440802333133

    Article  Google Scholar 

  • Osorio A, Fay S, Pouthas V, Ballesteros S (2010) Ageing affects brain activity in highly educated older adults: an ERP study using a word-stem priming task. Cortex 46:522–534. doi:10.1016/j.cortex.2009.09.003

    Article  PubMed  Google Scholar 

  • Park DC, Polk TA, Mikels JA, TaylorSF Marshuetz C (2001) Cerebral aging: integration of brain and behavioral models of cognitive function. Dialogues Clin Neurosci 3:151–165

    PubMed Central  CAS  PubMed  Google Scholar 

  • Park DC, Lautenschlager G, Hedden T, Davidson NS, Smith AD, Smith PK (2002) Models of visuospatial and verbal memory across the adult life span. Psychol Aging 17:299–320. doi:10.1037/0882-7974.17.2.299

    Article  PubMed  Google Scholar 

  • Persson J, Nyberg L, Lind J, Larsson A, Nilsson LG, Ingvar M, Buckner RL (2006) Structure-function correlates of cognitive decline in aging. Cereb Cortex 16:907–915

    Article  PubMed  Google Scholar 

  • Prull MW, Gabrieli JD, Bunge SA (2000) Age-related changes in memory: a cognitive neuroscience perspective. In: Salthouse (ed) The handbook of aging and cognition, 2nd edn. Mahwah, NJ, pp 91–153

  • Reales JM, Ballesteros S (1994) SDT_SP, a program in Pascal for computing parameters and significance tests from several detection theory designs. Behav Res Methods Instrum Comput 26:151–155

    Article  Google Scholar 

  • Redondo MT, Reales JM, Ballesteros S (2010) Memoria implícita y explícita en mayores no dementes con trastornos metabólicos producidos por la diabetes mellitus tipo 2. Psicológica 31:87–108

    Google Scholar 

  • Reijmer YD, Van den Berg E, De Bresser J, Kessels RP, Kappelle LJ et al (2011) Accelerated cognitive decline in patients with type 2 diabetes: MRI correlates and risk factors. Diabetes Metab Res Rev 27:195–202. doi:10.1002/dmrr.1163

    Article  PubMed  Google Scholar 

  • Rönnlund M, Nilsson LG (2008) The magnitude, generality, and determinants of Flynn effects on forms of declarative memory and visuospatial ability: time-sequential analyses of data from a Swedish cohort study. Intelligence 36:192–209. doi:10.1016/j.intell.2007.05.002

    Article  Google Scholar 

  • Rönnlund M, Nyberg L, Bäckman L, Nilsson G (2005) Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychol Aging 20:3–18. doi:10.1037/0882-7974.20.1.3

    Article  PubMed  Google Scholar 

  • Schacter D (1987) Implicit memory: history and current status. J Exp Psychol Learn 13:501–518

    Article  Google Scholar 

  • Spaan PE, Raaijmakers JG (2011) Priming effects from young-old to very old age on a word-stem completion task: minimizing explicit contamination. Aging Neuropsychol C 18:86–107. doi:10.1080/13825585.2010.511146

    Article  Google Scholar 

  • Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys and humans. Psychol Rev 99:195–213

    Article  CAS  PubMed  Google Scholar 

  • Squire LR (2004) Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82:171–177

    Article  PubMed  Google Scholar 

  • Stolk RP, Breteler MM, Ott A, Pols HA (1997) Insulin and cognitive function in an elderly population: the Rotterdam study. Diabetes Care 20:792–796

    Article  CAS  PubMed  Google Scholar 

  • Van den Berg E, Kloppenborg RP, Kessels RP, Kappelle LJ, Biessels GJ (2009) Type 2 diabetes mellitus, hypertension, dyslipidemia and obesity: a systematic comparison of their impact on cognition. Biochim Biophys Acta 1792:470–481

    Article  PubMed  Google Scholar 

  • Van den Berg E, Reijmer YD, De Bresser J, Kessels RP, Kappelle LJ, Biessels GJ (2010) A 4 follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia 53:58–65

    Article  PubMed Central  PubMed  Google Scholar 

  • Verdelho A, Madureira C, Moleiro JM, Ferro CO, Santos T et al (2010) White matter changes and diabetes predict cognitive decline in the elderly: the LADIS study. Neurology 75:160–167

    Article  CAS  PubMed  Google Scholar 

  • Wiggs C, Weisberg J, Martin A (2006) Repetition priming across the adult lifespan: the long and short of it. Aging Neurospsychol Cogn 13:308–325. doi:10.1080/138255890968718

    Article  Google Scholar 

  • Yaffe K, Falvey C, Hamilton N, Schwartz AV, Simonsick EM, Satterfield S, Cauley JA, Harris TB (2012) Diabetes, glucose control, and 9-year cognitive decline among older adults without dementia. Arch Neurol 69:1170–1175. doi:10.1001/archneurol.2012.1117

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was partially supported by grants from the Elche Hospital Foundation for Biomedical Research (Proyecto fibelx 09/08) and by the Spanish Government (PSI2013-41409-R) and the Madrid Community Biomedical Research Grant (S2010/BMD-2349). The authors thank all the volunteers who participated in the study. We are grateful to Drs. Miquel Baquero, Daniel Martín, Maribel Pérez and the medical staff of the health centers of Elche for their help in the recruitment of the participants. Finally, we are very grateful to two anonymous reviewers for their helpful and very constructive comments that helped us to improve the article. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Soledad Ballesteros.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Appendix

Appendix

See Table 3.

Table 3 Word list

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Redondo, M.T., Beltrán-Brotóns, J.L., Reales, J.M. et al. Word-stem priming and recognition in type 2 diabetes mellitus, Alzheimer’s disease patients and healthy older adults. Exp Brain Res 233, 3163–3174 (2015). https://doi.org/10.1007/s00221-015-4385-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-015-4385-7

Keywords

Navigation