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Brain Structure and Function

, Volume 220, Issue 3, pp 1555–1571 | Cite as

Specific and disease stage-dependent episodic memory-related brain activation patterns in Alzheimer’s disease: a coordinate-based meta-analysis

  • Nils Nellessen
  • Claudia Rottschy
  • Simon B. Eickhoff
  • Simon T. Ketteler
  • Hanna Kuhn
  • N. Jon Shah
  • Jörg B. Schulz
  • Martina Reske
  • Kathrin ReetzEmail author
Original Article

Abstract

Episodic memory is typically affected during the course of Alzheimer’s disease (AD). Due to the pronounced heterogeneity of functional neuroimaging studies on episodic memory impairments in mild cognitive impairment (MCI) and AD regarding their methodology and findings, we aimed to delineate consistent episodic memory-related brain activation patterns. We performed a systematic, quantitative, coordinate-based whole-brain activation likelihood estimation meta-analysis of 28 functional magnetic resonance imaging (fMRI) studies comprising 292 MCI and 102 AD patients contrasted to 409 age-matched control subjects. We included episodic encoding and/or retrieval phases, investigated the effects of group, verbal or image stimuli and correlated mean Mini-Mental-Status-Examination (MMSE) scores with the modelled activation estimates. MCI patients presented increased right hippocampal activation during memory encoding, decreased activation in the left hippocampus and fusiform gyrus during retrieval tasks, as well as attenuated activation in the right anterior insula/inferior frontal gyrus during verbal retrieval. In AD patients, however, stronger activation within the precuneus during encoding tasks was accompanied by attenuated right hippocampal activation during retrieval tasks. Low cognitive performance (MMSE scores) was associated with stronger activation of the precuneus and reduced activation of the right (para)hippocampus and anterior insula/inferior frontal gyrus. This meta-analysis provides evidence for a specific and probably disease stage-dependent brain activation pattern related to the pathognomonic AD characteristic of episodic memory loss.

Keywords

Alzheimer’s disease Mild cognitive impairment Episodic memory Functional neuroimaging Meta-analysis Hippocampus 

Notes

Acknowledgments

We would like to thank B. Hampstead for sharing additional data which lead to the inclusion of one further study (Hampstead et al. 2011). We would like to furthermore thank Imis Dogan for her invaluable input during our data investigation, Ana Costa for providing knowledge and relevant literature about the different human memory systems and Melissa Chung for proofreading the manuscript. NJS and JBS are in part funded by the Helmholtz Alliance ICEMED - Imaging and Curing Environmental Metabolic Diseases, through the Initiative and Network Fund of the Helmholtz Association. SBE was funded by the Human Brain Project (R01-MH074457-01A1) and acknowledges funding by the Initiative and Networking Fund of the Helmholtz Association within the Helmholtz Alliance on Systems Biology (Human Brain Model) and the IRTG 1328. SBE and KR were funded by the Excellence Initiative of the German federal and state governments.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

429_2014_744_MOESM1_ESM.docx (42 kb)
Supplementary material 1 (DOCX 41 kb)

References

  1. Bäckman L, Andersson JLR, Nyberg L et al (1999) Brain regions associated with episodic retrieval in normal aging and Alzheimer’ s disease. NeurologyGoogle Scholar
  2. Belleville S, Clément F, Mellah S et al (2011) Training-related brain plasticity in subjects at risk of developing Alzheimer’s disease. Brain 134:1623–1634. doi: 10.1093/brain/awr037 CrossRefPubMedGoogle Scholar
  3. Bokde ALW, Lopez-Bayo P, Meindl T et al (2006) Functional connectivity of the fusiform gyrus during a face-matching task in subjects with mild cognitive impairment. Brain 129:1113–1124. doi: 10.1093/brain/awl051 CrossRefPubMedGoogle Scholar
  4. Bokde ALW, Karmann M, Born C et al (2010) Altered brain activation during a verbal working memory task in subjects with amnestic mild cognitive impairment. J Alzheimers Dis 21:103–118. doi: 10.3233/JAD-2010-091054 PubMedGoogle Scholar
  5. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259CrossRefPubMedGoogle Scholar
  6. Braak H, Alafuzoff I, Arzberger T et al (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112:389–404. doi: 10.1007/s00401-006-0127-z CrossRefPubMedCentralPubMedGoogle Scholar
  7. Browndyke JN, Giovanello K, Petrella J et al (2012) Phenotypic regional functional imaging patterns during memory encoding in mild cognitive impairment and Alzheimer’s disease. Alzheimers Dement 9:284–294. doi: 10.1016/j.jalz.2011.12.006 CrossRefPubMedCentralPubMedGoogle Scholar
  8. Buckner RL, Raichle ME, Miezin FM, Petersen SE (1996) Functional anatomic studies of memory retrieval for auditory words and visual pictures. J Neurosci 16:6219–6235PubMedGoogle Scholar
  9. Buckner RL, Snyder AZ, Shannon BJ et al (2005) Molecular, structural, and functional characterization of Alzheimer’s disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci 25:7709–7717. doi: 10.1523/JNEUROSCI.2177-05.2005 CrossRefPubMedGoogle Scholar
  10. 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. doi: 10.1006/nimg.2002.1063 CrossRefPubMedGoogle Scholar
  11. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583. doi: 10.1093/brain/awl004 CrossRefPubMedGoogle Scholar
  12. Celone KA, Calhoun VD, Dickerson BC et al (2006) Alterations in memory networks in mild cognitive impairment and Alzheimer’s disease: an independent component analysis. J Neurosci 26:10222–10231. doi: 10.1523/JNEUROSCI.2250-06.2006 CrossRefPubMedGoogle Scholar
  13. Clément F, Belleville S (2010) Compensation and disease severity on the memory-related activations in mild cognitive impairment. Biol Psychiatry 68:894–902. doi: 10.1016/j.biopsych.2010.02.004 CrossRefPubMedGoogle Scholar
  14. Clément F, Belleville S (2012) Effect of disease severity on neural compensation of item and associative recognition in mild cognitive impairment. J Alzheimers Dis 29:109–123. doi: 10.3233/JAD-2011-110426 PubMedGoogle Scholar
  15. Clément F, Belleville S, Mellah S (2010) Functional neuroanatomy of the encoding and retrieval processes of verbal episodic memory in MCI. Cortex 46:1005–1015. doi: 10.1016/j.cortex.2009.07.003 CrossRefPubMedGoogle Scholar
  16. Dannhauser TM, Shergill SS, Stevens T et al (2008) An fMRI study of verbal episodic memory encoding in amnestic mild cognitive impairment. Cortex 44:869–880. doi: 10.1016/j.cortex.2007.04.005 CrossRefPubMedGoogle Scholar
  17. Dere E, Pause BM, Pietrowsky R (2010) Emotion and episodic memory in neuropsychiatric disorders. Behav Brain Res 215:162–171. doi: 10.1016/j.bbr.2010.03.017 CrossRefPubMedGoogle Scholar
  18. Derflinger S, Sorg C, Gaser C et al (2011) Grey-matter atrophy in Alzheimer’s disease is asymmetric but not lateralized. J Alzheimers Dis 25:347–357. doi: 10.3233/JAD-2011-110041 PubMedGoogle Scholar
  19. Dubois B, Feldman HH, Jacova C et al (2010) Revising the definition of Alzheimer’s disease: a new lexicon. Lancet Neurol 9:1118–1127. doi: 10.1016/S1474-4422(10)70223-4 CrossRefPubMedGoogle Scholar
  20. Duvernoy H, Cattin F, Naidich T et al (2005) Sectional anatomy and magnetic resonance imaging. In: Duvernoy HM (ed) Hum. Hippocampus, 3rd edn. Springer, Heidelberg, pp 129–217Google Scholar
  21. Eickhoff SB, Stephan KE, Mohlberg H et al (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335. doi: 10.1016/j.neuroimage.2004.12.034 CrossRefPubMedGoogle Scholar
  22. Eickhoff SB, Paus T, Caspers S et al (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511–521. doi: 10.1016/j.neuroimage.2007.03.060 CrossRefPubMedGoogle Scholar
  23. Eickhoff SB, Laird AR, Grefkes C et al (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926. doi: 10.1002/hbm.20718 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Eickhoff SB, Bzdok D, Laird AR et al (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59:2349–2361. doi: 10.1016/j.neuroimage.2011.09.017 CrossRefPubMedCentralPubMedGoogle Scholar
  25. Espinosa A, Alegret M, Valero S et al (2013) A longitudinal follow-up of 550 mild cognitive impairment patients: evidence for large conversion to dementia rates and detection of major risk factors involved. J Alzheimers Dis 34:769–780. doi: 10.3233/JAD-122002 PubMedGoogle Scholar
  26. 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. doi: 10.1016/0022-3956(75)90026-6 CrossRefPubMedGoogle Scholar
  27. Frings L, Dressel K, Abel S et al (2010) Reduced precuneus deactivation during object naming in patients with mild cognitive impairment, Alzheimer’s disease, and frontotemporal lobar degeneration. Dement Gerieatr Cogn 30:334–343. doi: 10.1159/000320991 CrossRefGoogle Scholar
  28. Giovanello KS, De Brigard F, Hennessey Ford J et al (2012) Event-related functional magnetic resonance imaging changes during relational retrieval in normal aging and amnestic mild cognitive impairment. J Int Neuropsychol Soc 18:886–897. doi: 10.1017/S1355617712000689 CrossRefPubMedGoogle Scholar
  29. Golby A, Silverberg G, Race E et al (2005) Memory encoding in Alzheimer’s disease: an fMRI study of explicit and implicit memory. Brain 128:773–787. doi: 10.1093/brain/awh400 CrossRefPubMedGoogle Scholar
  30. Golby AJ, Poldrack RA, Brewer JB et al (2001) Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain 124:1841–1854CrossRefPubMedGoogle Scholar
  31. Gould RL, Brown RG, Owen AM et al (2005) Functional neuroanatomy of successful paired associate learning in Alzheimer’s disease. Am J Psychiatry 162:2049–2060CrossRefPubMedGoogle Scholar
  32. Grady C (2012) The cognitive neuroscience of ageing. Nat Rev Neurosci 13:491–505. doi: 10.1038/nrn3256 CrossRefPubMedCentralPubMedGoogle Scholar
  33. Grön G, Bittner D, Schmitz B et al (2002) Subjective memory complaints: objective neural markers in patients with Alzheimer’s disease and major depressive disorder. Ann Neurol 51:491–498. doi: 10.1002/ana.10157 CrossRefPubMedGoogle Scholar
  34. Gusnard DA, Raichle ME (2001) Searching for a baseline: functional imaging and the resting human brain. Nat Rev Neurosci 2:685–694CrossRefPubMedGoogle Scholar
  35. Hämäläinen A, Pihlajamäki M, Tanila H et al (2007) Increased fMRI responses during encoding in mild cognitive impairment. Neurobiol Aging 28:1889–1903. doi: 10.1016/j.neurobiolaging.2006.08.008 CrossRefPubMedGoogle Scholar
  36. Hampstead BM, Stringer AY, Stilla RF et al (2011) Where did I put that? Patients with amnestic mild cognitive impairment demonstrate widespread reductions in activity during the encoding of ecologically relevant object-location associations. Neuropsychologia 49:2349–2361. doi: 10.1016/j.neuropsychologia.2011.04.008 CrossRefPubMedCentralPubMedGoogle Scholar
  37. Hanseeuw B, Dricot L, Kavec M et al (2011) Associative encoding deficits in amnestic mild cognitive impairment: a volumetric and functional MRI study. Neuroimage 56:1743–1748. doi: 10.1016/j.neuroimage.2011.03.034 CrossRefPubMedGoogle Scholar
  38. Hashimoto M, Masliah E (2003) Cycles of aberrant synaptic sprouting and neurodegeneration in Alzheimer’s and dementia with Lewy bodies. Neurochem Res 28:1743–1756CrossRefPubMedGoogle Scholar
  39. Hayes SM, Ryan L, Schnyer DM, Nadel L (2004) An fMRI study of episodic memory: retrieval of object, spatial, and temporal information. Behav Neurosci 118:885–896. doi: 10.1037/0735-7044.118.5.885 CrossRefPubMedCentralPubMedGoogle Scholar
  40. Heun R, Freymann K, Erb M et al (2007) Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly. Neurobiol Aging 28:404–413. doi: 10.1016/j.neurobiolaging.2006.01.012 CrossRefPubMedGoogle Scholar
  41. Huijbers W, Vannini P, Sperling RA et al (2012) Explaining the encoding/retrieval flip: memory-related deactivations and activations in the posteromedial cortex. Neuropsychologia 50:3764–3774. doi: 10.1016/j.neuropsychologia.2012.08.021 CrossRefPubMedGoogle Scholar
  42. Hynd MR, Scott HL, Dodd PR (2004) Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer’s disease. Neurochem Int 45:583–595. doi: 10.1016/j.neuint.2004.03.007 CrossRefPubMedGoogle Scholar
  43. Ikonomovic MD, Klunk WE, Abrahamson EE et al (2011) Precuneus amyloid burden is associated with reduced cholinergic activity in Alzheimer disease. Neurology 77:39–47. doi: 10.1212/WNL.0b013e3182231419 CrossRefPubMedCentralPubMedGoogle Scholar
  44. Jin M, Pelak VS, Curran T et al (2012) A preliminary study of functional abnormalities in aMCI subjects during different episodic memory tasks. Magn Reson Imaging 30:459–470. doi: 10.1016/j.mri.2011.12.014 CrossRefPubMedCentralPubMedGoogle Scholar
  45. Jonides J, Wager T, Badre DT (2002) Memory, neuroimaging. In: Ramachandran VS (ed) Encycl. Hum. Brain. Elsevier Science, San Diego, pp 797–833Google Scholar
  46. Jungwirth S, Zehetmayer S, Hinterberger M et al (2012) The validity of amnestic MCI and non-amnestic MCI at age 75 in the prediction of Alzheimer’s dementia and vascular dementia. Int Psychogeriatr 24:959–966. doi: 10.1017/S1041610211002870 CrossRefPubMedGoogle Scholar
  47. Kelley WM, Miezin FM, McDermott KB et al (1998) Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron 20:927–936CrossRefPubMedGoogle Scholar
  48. Kircher TT, Weis S, Freymann K et al (2007) Hippocampal activation in patients with mild cognitive impairment is necessary for successful memory encoding. J Neurol Neurosurg Psychiatry 78:812–818. doi: 10.1136/jnnp.2006.104877 CrossRefPubMedCentralPubMedGoogle Scholar
  49. Kochan N, Breakspear M, Slavin MJ et al (2010) Functional alterations in brain activation and deactivation in mild cognitive impairment in response to a graded working memory challenge. Dement Geriatr Cogn 30:553–568. doi: 10.1159/000322112 CrossRefGoogle Scholar
  50. Kühn S, Gallinat J (2013) Segregating cognitive functions within hippocampal formation: a quantitative meta-analysis on spatial navigation and episodic memory. Hum Brain Mapp. doi: 10.1002/hbm.22239
  51. Kurth F, Zilles K, Fox PT et al (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534. doi: 10.1007/s00429-010-0255-z CrossRefPubMedGoogle Scholar
  52. Laird AR, Eickhoff SB, Kurth F et al (2009) ALE meta-analysis workflows via the brainmap database: progress towards a probabilistic functional brain atlas. Front Neuroinform 3:11. doi: 10.3389/neuro.11.023.2009 CrossRefGoogle Scholar
  53. Lim TS, Lee HY, Barton JJS, Moon SY (2011) Deficits in face perception in the amnestic form of mild cognitive impairment. J Neurol Sci 309:123–127. doi: 10.1016/j.jns.2011.07.001 CrossRefPubMedGoogle Scholar
  54. Machulda MM, Senjem ML, Weigand SD et al (2009) Functional MRI changes in amnestic and non-amnestic MCI during encoding and recognition tasks. J Int Neuropsychol Soc 15:372–382. doi: 10.1017/S1355617709090523 CrossRefPubMedCentralPubMedGoogle Scholar
  55. Mandzia JL, McAndrews MP, Grady CL et al (2009) Neural correlates of incidental memory in mild cognitive impairment: an fMRI study. Neurobiol Aging 30:717–730. doi: 10.1016/j.neurobiolaging.2007.08.024 CrossRefPubMedGoogle Scholar
  56. McCarthy G, Blamire AM, Rothman DL et al (1993) Echo-planar magnetic resonance imaging studies of frontal cortex activation during word generation in humans. Proc Natl Acad Sci USA 90:4952–4956CrossRefPubMedCentralPubMedGoogle Scholar
  57. McCarthy G, Puce A, Gore JC, Allison T (1996) Face-specific processing in the human fusiforrn gyms. J Cogn Neurosci 9:605–610CrossRefGoogle Scholar
  58. McKhann G, Drachman D, Folstein M et al (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34:939–944CrossRefPubMedGoogle Scholar
  59. Mueller SG, Schuff N, Yaffe K et al (2010) Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer’s disease. Hum Brain Mapp 31:1339–1347. doi: 10.1002/hbm.20934 CrossRefPubMedCentralPubMedGoogle Scholar
  60. Nickl-Jockschat T, Kleiman A, Schulz JB et al (2012) Neuroanatomic changes and their association with cognitive decline in mild cognitive impairment: a meta-analysis. Brain Struct Funct 217:115–125. doi: 10.1007/s00429-011-0333-x CrossRefPubMedGoogle Scholar
  61. Nyberg L, McIntosh AR, Houle S et al (1996) Activation of medial temporal structures during episodic memory retrieval. Nature 380:715–717. doi: 10.1038/380715a0 CrossRefPubMedGoogle Scholar
  62. O’Brien JL, O’Keefe K, LaViolette PS et al (2010) Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology 74:1969–1976CrossRefPubMedCentralPubMedGoogle Scholar
  63. Palop JJ, Chin J, Roberson ED et al (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer’s disease. Neuron 55:697–711. doi: 10.1016/j.neuron.2007.07.025 CrossRefPubMedGoogle Scholar
  64. Pariente J, Cole S, Henson R et al (2005) Alzheimer’s patients engage an alternative network during a memory task. Ann Neurol 58:870–879. doi: 10.1002/ana.20653 CrossRefPubMedGoogle Scholar
  65. Pause BM, Zlomuzica A, Kinugawa K et al (2013) Perspectives on episodic-like and episodic memory. Front Behav Neurosci 7:33. doi: 10.3389/fnbeh.2013.00033 CrossRefPubMedCentralPubMedGoogle Scholar
  66. Peters F, Collette F, Degueldre C et al (2009) The neural correlates of verbal short-term memory in Alzheimer’s disease: an fMRI study. Brain 132:1833–1846. doi: 10.1093/brain/awp075 CrossRefPubMedGoogle Scholar
  67. Petersen RC (2011) Mild cognitive impairment. N Engl J Med 364:2227–2234CrossRefPubMedGoogle Scholar
  68. Petersen RC, Smith GE, Waring SC et al (1999) Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56:303–308CrossRefPubMedGoogle Scholar
  69. Petrella JR, Krishnan S, Slavin MJ et al (2006) Mild cognitive impairment: evaluation with 4-T functional MR imaging. Radiology 240:177–186Google Scholar
  70. Petrella JR, Prince SE, Wang L et al (2007) Prognostic value of posteromedial cortex deactivation in mild cognitive impairment. PLoS ONE 2:e1104. doi: 10.1371/journal.pone.0001104 CrossRefPubMedCentralPubMedGoogle Scholar
  71. Price CJ (2000) The anatomy of language: contributions from functional neuroimaging. J Anat 197:335–359CrossRefPubMedCentralPubMedGoogle Scholar
  72. Price CJ (2010) The anatomy of language: a review of 100 fMRI studies published in 2009. Ann NY Acad Sci 1191:62–88. doi: 10.1111/j.1749-6632.2010.05444.x CrossRefPubMedGoogle Scholar
  73. Rémy F, Mirrashed F, Campbell B, Richter W (2005) Verbal episodic memory impairment in Alzheimer’s disease: a combined structural and functional MRI study. Neuroimage 25:253–266. doi: 10.1016/j.neuroimage.2004.10.045 Google Scholar
  74. Rosazza C, Minati L, Ghielmetti F et al (2009) Engagement of the medial temporal lobe in verbal and nonverbal memory: assessment with functional MR imaging in healthy subjects. Am J Neuroradiol 30:1134–1141. doi: 10.3174/ajnr.A1518 CrossRefPubMedGoogle Scholar
  75. Salehi A, Swaab DF (1999) Diminished neuronal metabolic activity in Alzheimer’s disease. Review article. J Neural Transm 106:955–986CrossRefPubMedGoogle Scholar
  76. Schacter DL, Curran T, Reiman EM et al (1999) Medial temporal lobe activation during episodic encoding and retrieval: a PET study. Hippocampus 9:575–881. doi: 10.1002/(SICI)1098-1063(1999)9:5<575:AID-HIPO11>3.0.CO;2-K CrossRefPubMedGoogle Scholar
  77. Scheff SW, Price DA, Schmitt FA et al (2013) Synapse stability in the precuneus early in the progression of Alzheimer’s disease. J Alzheimers Dis 35:599–609. doi: 10.3233/JAD-122353 PubMedCentralPubMedGoogle Scholar
  78. Schilbach L, Bzdok D, Timmermans B et al (2012) Introspective minds: using ALE meta-analyses to study commonalities in the neural correlates of emotional processing, social & unconstrained cognition. PLoS ONE 7:e30920. doi: 10.1371/journal.pone.0030920 CrossRefPubMedCentralPubMedGoogle Scholar
  79. Schroeter ML, Stein T, Maslowski N, Neumann J (2009) Neural correlates of Alzheimer’s disease and mild cognitive impairment: a systematic and quantitative meta-analysis involving 1351 patients. Neuroimage 47:1196–1206. doi: 10.1016/j.neuroimage.2009.05.037 CrossRefPubMedCentralPubMedGoogle Scholar
  80. Schwindt GC, Black SE (2009) Functional imaging studies of episodic memory in Alzheimer’s disease: a quantitative meta-analysis. Neuroimage 45:181–190. doi: 10.1016/j.neuroimage.2008.11.024 CrossRefPubMedGoogle Scholar
  81. Scoville WB, Milner B (2000) Loss of recent memory after bilateral hippocampal lesions. J Neuropsych Clin Neurosci 12:103–113CrossRefGoogle Scholar
  82. Small SA, Schobel SA, Buxton RB et al (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12:585–601. doi: 10.1038/nrn3085 CrossRefPubMedCentralPubMedGoogle Scholar
  83. Spaniol J, Davidson PSR, Kim ASN et al (2009) Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 47:1765–1779. doi: 10.1016/j.neuropsychologia.2009.02.028 CrossRefPubMedGoogle Scholar
  84. Sperling RA, Bates JF, Chua EF et al (2003) fMRI studies of associative encoding in young and elderly controls and mild Alzheimer’s disease. J Neurol Neurosurg Psychiatry 74:44–50Google Scholar
  85. Sperling RA, Laviolette PS, O’Keefe K et al (2009) Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63:178–188. doi: 10.1016/j.neuron.2009.07.003 CrossRefPubMedCentralPubMedGoogle Scholar
  86. Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306. doi: 10.1146/annurev.neuro.27.070203.144130 CrossRefPubMedGoogle Scholar
  87. Stark CE, Squire LR (2001) When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci USA 98:12760–12766. doi: 10.1073/pnas.221462998 CrossRefPubMedCentralPubMedGoogle Scholar
  88. Trivedi MA, Murphy CM, Goetz C et al (2008) fMRI activation changes during successful episodic memory encoding and recognition in amnestic mild cognitive impairment relative to cognitively healthy older adults. Dement Geriatr Cogn Disord 26:123–137. doi: 10.1159/000148190 CrossRefPubMedCentralPubMedGoogle Scholar
  89. Tulving E (1972) Episodic and semantic memory. In: Tulving E (ed) Organ. Mem. Academic Press, New York, pp 381–403Google Scholar
  90. Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA (2002) Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 16:765–780. doi: 10.1006/nimg.2002.1131 CrossRefPubMedGoogle Scholar
  91. Turkeltaub PE, Eickhoff SB, Laird AR et al (2012) Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum Brain Mapp 33:1–13. doi: 10.1002/hbm.21186 CrossRefPubMedGoogle Scholar
  92. Van der Meulen M, Lederrey C, Rieger SW et al (2012) Associative and semantic memory deficits in amnestic mild cognitive impairment as revealed by functional magnetic resonance imaging. Cogn Behav Neurol 25:195–215Google Scholar
  93. Wang X, Han Z, He Y et al (2013) Where color rests: spontaneous brain activity of bilateral fusiform and lingual regions predicts object color knowledge performance. Neuroimage 76:252–263. doi: 10.1016/j.neuroimage.2013.03.010 CrossRefPubMedGoogle Scholar
  94. Welsh K, Butters N, Hughes J et al (1991) Detection of abnormal memory decline in mild cases of Alzheimer’s disease using CERAD neuropsychological measures. Arch Neurol Chicago 48:278–281CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Nils Nellessen
    • 1
    • 2
    • 3
  • Claudia Rottschy
    • 4
    • 5
  • Simon B. Eickhoff
    • 4
    • 6
  • Simon T. Ketteler
    • 1
    • 2
  • Hanna Kuhn
    • 1
    • 2
    • 3
  • N. Jon Shah
    • 1
    • 2
    • 3
  • Jörg B. Schulz
    • 1
    • 3
  • Martina Reske
    • 2
  • Kathrin Reetz
    • 1
    • 2
    • 3
    Email author
  1. 1.Department of NeurologyRWTH Aachen UniversityAachenGermany
  2. 2.Institute of Neuroscience and Medicine (INM-4)Forschungszentrum Jülich GmbHJülichGermany
  3. 3.Jülich Aachen Research Alliance (JARA), Translational Brain MedicineJülich, AachenGermany
  4. 4.Institute of Neuroscience and Medicine (INM-1)Forschungszentrum Jülich GmbHJülichGermany
  5. 5.Department of Psychiatry, Psychotherapy and PsychosomaticsRWTH Aachen UniversityAachenGermany
  6. 6.Institute of Clinical Neuroscience and Medical PsychologyHeinrich Heine UniversityDüsseldorfGermany

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