Brain Imaging and Behavior

, Volume 9, Issue 4, pp 776–789 | Cite as

The influence of age and mild cognitive impairment on associative memory performance and underlying brain networks

  • Christiane S. H. Oedekoven
  • Andreas Jansen
  • James L. Keidel
  • Tilo Kircher
  • Dirk Leube
Original Research


Associative memory is essential to everyday activities, such as the binding of faces and corresponding names to form single bits of information. However, this ability often becomes impaired with increasing age. The most important neural substrate of associative memory is the hippocampus, a structure crucially implicated in the pathogenesis of Alzheimer’s disease (AD). The main aim of this study was to compare neural correlates of associative memory in healthy aging and mild cognitive impairment (MCI), an at-risk state for AD. We used fMRI to investigate differences in brain activation and connectivity between young controls (n = 20), elderly controls (n = 32) and MCI patients (n = 21) during associative memory retrieval. We observed lower hippocampal activation in MCI patients than control groups during a face-name recognition task, and the magnitude of this decrement was correlated with lower associative memory performance. Further, increased activation in precentral regions in all older adults indicated a stronger involvement of the task positive network (TPN) with age. Finally, functional connectivity analysis revealed a stronger link of hippocampal and striatal components in older adults in comparison to young controls, regardless of memory impairment. In elderly controls, this went hand-in-hand with a stronger activation of striatal areas. Increased TPN activation may be linked to greater reliance on cognitive control in both older groups, while increased functional connectivity between the hippocampus and the striatum may suggest dedifferentiation, especially in elderly controls.


Aging Mild cognitive impairment (MCI) Hippocampus Task positive network (TPN) Functional connectivity 



We thank the volunteers for their time and their interest in research, and the core unit Brainimaging for their support. The study was funded by an intramural grant from the University Clinic Giessen and Marburg (Project Number 31/2009 MR).

Conflict of interest

Christiane S. H. Oedekoven, Andreas Jansen, James L. Keidel, Tilo Kircher, and Dirk Leube declare that they have no conflicts of interest with respect to the research, authorship, and/or publication of this article.

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients for being included in the study.


  1. 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(3), 270–279. doi: 10.1016/j.jalz.2011.03.008.CrossRefGoogle Scholar
  2. Anderson, N. D., Ebert, P. L., Jennings, J. M., Grady, C. L., Cabeza, R., & Graham, S. J. (2008). Recollection- and familiarity-based memory in healthy aging and amnestic mild cognitive impairment. Neuropsychology, 22(2), 177–187. doi: 10.1037/0894-4105.22.2.177.CrossRefPubMedGoogle Scholar
  3. Bäckman, L., Andersson, J. L., Nyberg, L., Winblad, B., Nordberg, A., & Almkvist, O. (1999). Brain regions associated with episodic retrieval in normal aging and Alzheimer’s disease. Neurology, 52(9), 1861–1870.CrossRefPubMedGoogle Scholar
  4. Bartrés-Faz, D., Serra-Grabulosa, J. M., Sun, F. T., Solé-Padullés, C., Rami, L., Molinuevo, J. L., & D’Esposito, M. (2008). Functional connectivity of the hippocampus in elderly with mild memory dysfunction carrying the APOE epsilon4 allele. Neurobiology of Aging, 29(11), 1644–1653. doi: 10.1016/j.neurobiolaging.2007.04.021.CrossRefPubMedGoogle Scholar
  5. Bernard, F. A., Bullmore, E. T., Graham, K. S., Thompson, S. A., Hodges, J. R., & Fletcher, P. C. (2004). The hippocampal region is involved in successful recognition of both remote and recent famous faces. NeuroImage, 22(4), 1704–1714. doi: 10.1016/j.neuroimage.2004.03.036.CrossRefPubMedGoogle Scholar
  6. Bird, C. M., & Burgess, N. (2008). The hippocampus and memory: insights from spatial processing. Nature Reviews. Neuroscience, 9(3), 182–194. doi: 10.1038/nrn2335.CrossRefPubMedGoogle Scholar
  7. Bokde, A. L. W., Ewers, M., & Hampel, H. (2009). Assessing neuronal networks: understanding Alzheimer’s disease. Progress in Neurobiology, 89(2), 125–133. doi: 10.1016/j.pneurobio.2009.06.004.CrossRefPubMedGoogle Scholar
  8. Burianova, H., McIntosh, A. R., & Grady, C. L. (2010). A common functional brain network for autobiographical, episodic, and semantic memory retrieval. NeuroImage, 49(1), 865–874. doi: 10.1016/j.neuroimage.2009.08.066.CrossRefPubMedGoogle Scholar
  9. Cabeza, R. E., & Dennis, N. A. (2012). “Frontal lobes and aging: deterioration and compensation,” in Principles of frontal lobe function, eds. Stuss, D. T. and Knight, R.885 T. (New York: Oxford University Press)Google Scholar
  10. Celone, K. A., Calhoun, V. D., Dickerson, B. C., Atri, A., Chua, E. F., Miller, S. L., & Sperling, R. A. (2006). Alterations in memory networks in mild cognitive impairment and Alzheimer’s disease: an independent component analysis. The Journal of Neuroscience, 26(40), 10222–10231. doi: 10.1523/JNEUROSCI. 2250-06.2006.CrossRefPubMedGoogle Scholar
  11. Cole, M. W., & Schneider, W. (2007). The cognitive control network: Integrated cortical regions with dissociable functions. NeuroImage, 37(1), 343–360. doi: 10.1016/j.neuroimage.2007.03.071.CrossRefPubMedGoogle Scholar
  12. Della-Maggiore, V., Sekuler, A. B., Grady, C. L., Bennett, P. J., Sekuler, R., & McIntosh, A. R. (2000). Corticolimbic interactions associated with performance on a short-term memory task are modified by age. The Journal of Neuroscience, 20(22), 8410–8416.PubMedGoogle Scholar
  13. Dennis, N. A., & Cabeza, R. E. (2008). Neuroimaging of healthy cognitive aging. In F. I. M. Craik & T. A. Salthouse (Eds.), Handbook of aging and cognition (pp. 1–54).Google Scholar
  14. Dennis, N. A., & Cabeza, R. (2011). Age-related dedifferentiation of learning systems: an fMRI study of implicit and explicit learning. Neurobiology of Aging, 32(12), 2318. doi: 10.1016/j.neurobiolaging.2010.04.004.PubMedCentralCrossRefPubMedGoogle Scholar
  15. Diana, R. A., Yonelinas, A. P., & Ranganath, C. (2007). Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends in Cognitive Sciences, 11(9), 379–386. doi: 10.1016/j.tics.2007.08.001.CrossRefPubMedGoogle Scholar
  16. Dickerson, B. C., Salat, D. H., Greve, D. N., Chua, E. F., Rand-Giovannetti, E., Rentz, D. M., & Sperling, R. A. (2005). Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology, 65(3), 404–411. doi: 10.1212/01.wnl.0000171450.97464.49.PubMedCentralCrossRefPubMedGoogle Scholar
  17. Dickerson, B. C., & Eichenbaum, H. (2010). The episodic memory system: neurocircuitry and disorders. Neuropsychopharmacology, 35(1), 86–104. doi: 10.1038/npp.2009.126.PubMedCentralCrossRefPubMedGoogle Scholar
  18. Dickerson, B. C., Salat, D. H., Bates, J. F., Atiya, M., Killiany, R. J., Greve, D. N., & Sperling, R. A. (2004). Medial temporal lobe function and structure in mild cognitive impairment. Annals of Neurology, 56(1), 27–35. doi: 10.1002/ana.20163.PubMedCentralCrossRefPubMedGoogle Scholar
  19. Dickerson, B. C., & Sperling, R. A. (2008). Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer’s disease: insights from functional MRI studies. Neuropsychologia, 46(6), 1624–1635. doi: 10.1016/j.neuropsychologia.2007.11.030.PubMedCentralCrossRefPubMedGoogle Scholar
  20. Doeller, C. F., King, J. A., & Burgess, N. (2008). Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proceedings of the National Academy of Sciences of the United States of America, 105, 5915–5920. doi: 10.1073/pnas.0801489105.PubMedCentralCrossRefPubMedGoogle Scholar
  21. Eickhoff, S., Stephan, K. E., Mohlberg, H., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage, 25, 1325–1335.CrossRefPubMedGoogle Scholar
  22. Erk, S., Spottke, A., Meisen, A., Wagner, M., Walter, H., & Jessen, F. (2011). Evidence of neuronal compensation during episodic memory in subjective memory impairment. Archives of General Psychiatry, 68(8), 845–852. doi: 10.1001/archgenpsychiatry.2011.80.CrossRefPubMedGoogle Scholar
  23. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 9673–9678. doi: 10.1073/pnas.0504136102.PubMedCentralCrossRefPubMedGoogle Scholar
  24. Grady, C. L. (2008). Cognitive neuroscience of aging. Annals of the New York Academy of Sciences, 1124(C), 127–144. doi: 10.1196/annals.1440.009.CrossRefPubMedGoogle Scholar
  25. Grady, C. L. (2012). The cognitive neuroscience of ageing. Nature Reviews. Neuroscience, 13, 491–505. doi: 10.1038/nrn3256.PubMedCentralCrossRefPubMedGoogle Scholar
  26. Grady, C. L., Protzner, A. B., Kovacevic, N., Strother, S. C., Afshin-Pour, B., Wojtowicz, M., & McIntosh, A. R. (2010). A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. Cerebral Cortex, 20(6), 1432–1447. doi: 10.1093/cercor/bhp207.PubMedCentralCrossRefPubMedGoogle Scholar
  27. Hartley, T., Maguire, E. A., Spiers, H. J., & Burgess, N. (2003). The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron, 37, 877–888.CrossRefPubMedGoogle Scholar
  28. Irish, M., Lawlor, B. A., Coen, R. F., & O’Mara, S. M. (2011). Everyday episodic memory in amnestic mild cognitive impairment: a preliminary investigation. BMC Neuroscience, 12(1), 80. doi: 10.1186/1471-2202-12-80.PubMedCentralCrossRefPubMedGoogle Scholar
  29. Johnson, S. C., Schmitz, T. W., Moritz, C. H., Meyerand, M. E., Rowley, H. A., Alexander, A. L., & Alexander, G. E. (2006). Activation of brain regions vulnerable to Alzheimer’s disease: the effect of mild cognitive impairment. Neurobiology of Aging, 27(11), 1604–1612. doi: 10.1016/j.neurobiolaging.2005.09.017.PubMedCentralCrossRefPubMedGoogle Scholar
  30. Kim, H., Daselaar, S. M., & Cabeza, R. (2010). Overlapping brain activity between episodic memory encoding and retrieval: roles of the task-positive and task-negative networks. NeuroImage, 49(1), 1045–1054. doi: 10.1016/j.neuroimage.2009.07.058.PubMedCentralCrossRefPubMedGoogle Scholar
  31. Kircher, T., Weis, S., Leube, D., Freymann, K., Erb, M., Jessen, F., & Krach, S. (2008). Anterior hippocampus orchestrates successful encoding and retrieval of non-relational memory: an event-related fMRI study. European Archives of Psychiatry and Clinical Neuroscience, 258(6), 363–372. doi: 10.1007/s00406-008-0805-z.CrossRefPubMedGoogle Scholar
  32. Kirwan, C. B., & Stark, C. E. L. (2004). Medial temporal lobe activation during encoding and retrieval of novel face-name pairs. Hippocampus, 14(7), 919–930. doi: 10.1002/hipo.20014.PubMedCentralCrossRefPubMedGoogle Scholar
  33. Langenecker, S. A., Briceno, E. M., Hamid, N. M., & Nielson, K. A. (2007). An evaluation of distinct volumetric and functional MRI contributions toward understanding age and task performance: a study in the basal ganglia. Brain Research, 1135(1), 58–68. doi: 10.1016/j.brainres.2006.11.068.PubMedCentralCrossRefPubMedGoogle Scholar
  34. Li, K. Z. H., & Lindenberger, U. (2002). Relations between aging sensory/sensorimotor and cognitive functions. Neuroscience and Biobehavioral Reviews, 26, 777–783.CrossRefPubMedGoogle Scholar
  35. Lustig, C., Snyder, A. Z., Bhakta, M., O’Brien, K. C., McAvoy, M., Raichle, M. E., & Buckner, R. L. (2003). Functional deactivations: change with age and dementia of the Alzheimer type. Proceedings of the National Academy of Sciences of the United States of America, 100(24), 14504–14509. doi: 10.1073/pnas.2235925100.PubMedCentralCrossRefPubMedGoogle Scholar
  36. Machulda, M. M., Ward, H. A., Borowski, B., Gunter, J. L., Cha, R. H., O’Brien, P. C., & Jack, C. R. (2003). Comparison of memory fMRI response among normal, MCI, and Alzheimer’s patients. Neurology, 61(4), 500–506.PubMedCentralCrossRefPubMedGoogle Scholar
  37. Mayes, A., Montaldi, D., & Migo, E. (2007). Associative memory and the medial temporal lobes. Trends in Cognitive Sciences, 11(3), 126–135. doi: 10.1016/j.tics.2006.12.003.CrossRefPubMedGoogle Scholar
  38. McCormick, C., Moscovitch, M., Protzner, A. B., Huber, C. G., & McAndrews, M. P. (2010). Hippocampal-neocortical networks differ during encoding and retrieval of relational memory: functional and effective connectivity analyses. Neuropsychologia, 48(11), 3272–3281. doi: 10.1016/j.neuropsychologia.2010.07.010.CrossRefPubMedGoogle Scholar
  39. Minear, M., & Park, D. C. (2004). A lifespan database of adult facial stimuli. Behavior Research Methods, Instruments, & Computers, 36(4), 630–633.CrossRefGoogle Scholar
  40. Morcom, A. M., Li, J., & Rugg, M. D. (2007). Age effects on the neural correlates of episodic retrieval: increased cortical recruitment with matched performance. Cerebral Cortex, 17(11), 2491–2506. doi: 10.1093/cercor/bhl155.CrossRefPubMedGoogle Scholar
  41. Naveh-Benjamin, M. (2000). Adult age differences in memory performance: tests of an associative deficit hypothesis. Journal of Experimental Psychology Learning, 26, 1170–1187.CrossRefGoogle Scholar
  42. Naveh-Benjamin, M., Guez, J., Kilb, A., & Reedy, S. (2004). The associative memory deficit of older adults: further support using face-name associations. Psychology and Aging, 19(3), 541–546. doi: 10.1037/0882-7974.19.3.541.CrossRefPubMedGoogle Scholar
  43. O’Brien, J. L., O’Keefe, K. M., LaViolette, P. S., DeLuca, A. N., Blacker, D., Dickerson, B. C., & Sperling, R. A. (2010). Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology, 74(24), 1969–1976. doi: 10.1212/WNL.0b013e3181e3966e.PubMedCentralCrossRefPubMedGoogle Scholar
  44. Oedekoven, C. S. H., Jansen, A., Kircher, T. T., & Leube, D. T. (2013). Age-related changes in parietal lobe activation during an episodic memory retrieval task. Journal of Neural Transmission, 120(5), 799–806. doi: 10.1007/s00702-012-0904-x.CrossRefPubMedGoogle Scholar
  45. Old, S. R., & Naveh-Benjamin, M. (2008). Differential effects of age on item and associative measures of memory: a meta-analysis. Psychology and Aging, 23(1), 104–118. doi: 10.1037/0882-7974.23.1.104.CrossRefPubMedGoogle Scholar
  46. Pariente, J., Cole, S., Henson, R., Clare, L., Kennedy, A., Rossor, M., & Frackowiak, R. S. J. (2005). Alzheimer’s patients engage an alternative network during a memory task. Annals of Neurology, 58(6), 870–879. doi: 10.1002/ana.20653.CrossRefPubMedGoogle Scholar
  47. Paulus, F. M., Krach, S., Bedenbender, J., Pyka, M., Sommer, J., Krug, A., & Jansen, A. (2013). Partial support for ZNF804A genotype-dependent alterations in prefrontal connectivity. Human Brain Mapping, 34(2), 304–313. doi: 10.1002/hbm.21434.CrossRefPubMedGoogle Scholar
  48. Persson, J., Kalpouzos, G., Nilsson, L.-G., Ryberg, M., & Nyberg, L. (2011). Preserved hippocampus activation in normal aging as revealed by fMRI. Hippocampus, 21(7), 753–766. doi: 10.1002/hipo.20794.CrossRefPubMedGoogle Scholar
  49. Petersen, R. C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256(3), 183–194. doi: 10.1111/j.1365-2796.2004.01388.x.CrossRefPubMedGoogle Scholar
  50. Petrella, J. R., Krishnan, S., Slavin, M. J., Tran, T. T., Murty, L., & Doraiswamy, P. M. (2006). Mild cognitive impairment: evaluation with 4-T functional MR imaging. Radiology, 240(1), 177–186. doi: 10.1148/radiol.2401050739.CrossRefPubMedGoogle Scholar
  51. Pike, K. E., Kinsella, G. J., Ong, B., Mullaly, E., Rand, E., Storey, E., & Parsons, S. (2012). Names and numberplates: quasi-everyday associative memory tasks for distinguishing amnestic mild cognitive impairment from healthy aging. Journal of Clinical and Experimental Neuropsychology, 34(3), 269–278. doi: 10.1080/13803395.2011.633498.CrossRefPubMedGoogle Scholar
  52. Pires, C., Silva, D., Maroco, J., Ginó, S., Mendes, T., Schmand, B. A., & de Mendonça, A. (2012). Memory complaints associated with seeking clinical care. International Journal of Alzheimer’s Disease, 2012, 725329. doi: 10.1155/2012/725329.PubMedCentralPubMedGoogle Scholar
  53. Poldrack, R. A., Clark, J., Pare-Blagoev, E. J., Shohamy, D., Creso Moyano, J., Myers, C., & Gluck, M. A. (2001). Interactive memory and learning systems in the human brain. Nature, 414, 546–550.CrossRefPubMedGoogle Scholar
  54. Price, C. J., & Friston, K. J. (1999). Scanning patients with tasks they can perform. Human Brain Mapping, 8(2–3), 102–108.CrossRefPubMedGoogle Scholar
  55. Raz, N., & Rodrigue, K. R. (2006). Differential aging of the brain: Patterns, cognitive correlates and modifiers. Neuroscience and Biobehavioral Reviews, 30, 730–748.CrossRefPubMedGoogle Scholar
  56. Reuter-Lorenz, P. A., & Park, D. C. (2010). Human neuroscience and the aging mind: a new look at old problems. The Journals of Gerontology Series B: Psychological Sciences and Social Sciences, 65(4), 405–415. doi: 10.1093/geronb/gbq035.CrossRefGoogle Scholar
  57. Rieckmann, A., Fischer, H., & Bäckman, L. (2010). Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: Relations to performance. NeuroImage, 50, 1303–1312. doi: 10.1016/j.neuroimage.2010.01.015.CrossRefPubMedGoogle Scholar
  58. Salami, A., Eriksson, J., & Nyberg, L. (2012). Opposing effects of aging on large-scale brain systems for memory encoding and cognitive control. The Journal of Neuroscience, 32(31), 10749–10757. doi: 10.1523/JNEUROSCI. 0278-12.2012.CrossRefPubMedGoogle Scholar
  59. Schuck, N. W., Doeller, C. F., Schjeide, B. M., Schröder, J., Frensch, P. A., Bertram, L., & Li, S. C. (2013). Aging and KIBRA/WWC1 genotype affect spatial memory processes in a virtual navigation task. Hippocampus, 23(10), 919–930.CrossRefPubMedGoogle Scholar
  60. Schwindt, G. C., & Black, S. E. (2009). Functional imaging studies of episodic memory in Alzheimer’s disease: a quantitative meta-analysis. NeuroImage, 45(1), 181–190. doi: 10.1016/j.neuroimage.2008.11.024.CrossRefPubMedGoogle Scholar
  61. Small, S. A., Nava, A. S., Perera, G. M., DeLaPaz, R., Mayeux, R., & Stern, Y. (2001). Circuit mechanisms underlying memory encoding and retrieval in the long axis of the hippocampal formation. Nature Neuroscience, 4(4), 442–449. doi: 10.1038/86115.CrossRefPubMedGoogle Scholar
  62. Sperling, R. A. (2003). fMRI studies of associative encoding in young and elderly controls and mild Alzheimer’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 74(1), 44–50. doi: 10.1136/jnnp.74.1.44.CrossRefGoogle Scholar
  63. Spreng, R. N., Wojtowicz, M., & Grady, C. L. (2010). Reliable differences in brain activity between young and old adults: a quantitative meta-analysis across multiple cognitive domains. Neuroscience and Biobehavioral Reviews, 34(8), 1178–1194. doi: 10.1016/j.neubiorev.2010.01.009.CrossRefPubMedGoogle Scholar
  64. Squire, L. R., & Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science, 253(5026), 1380–1386.CrossRefPubMedGoogle Scholar
  65. Toro, R., Fox, P. T., & Paus, T. (2008). Functional coactivation map of the human brain. Cerebral Cortex, 18(11), 2553–2559. doi: 10.1093/cercor/bhn014.PubMedCentralCrossRefPubMedGoogle Scholar
  66. Troyer, A. K., D’Souza, N. A., Vandermorris, S., & Murphy, K. J. (2011). Age-related differences in associative memory depend on the types of associations that are formed. Neuropsychology, Development, and Cognition. Section B, Aging, Neuropsychology and Cognition, 18(3), 340–352. doi: 10.1080/13825585.2011.553273.CrossRefPubMedGoogle Scholar
  67. Tsukiura, T., Sekiguchi, A., Yomogida, Y., Nakagawa, S., Shigemune, Y., Kambara, T., & Kawashima, R. (2011). Effects of aging on hippocampal and anterior temporal activations during successful retrieval of memory for face-name associations. Journal of Cognitive Neuroscience, 23(1), 200–213. doi: 10.1162/jocn.2010.21476.CrossRefPubMedGoogle Scholar
  68. Vannini, P., O’Brien, J., O’Keefe, K., Pihlajamaki, M., Laviolette, P., & Sperling, R. A. (2011). What goes down must come up: role of the posteromedial cortices in encoding and retrieval. Cerebral Cortex, 21(1), 22–34.PubMedCentralCrossRefPubMedGoogle Scholar
  69. Vincent, J. L., Kahn, I., Snyder, A. Z., Raichle, M. E., & Buckner, R. L. (2008). Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. Journal of Neurophysiology, 100(6), 3328–3342. doi: 10.1152/jn.90355.2008.PubMedCentralCrossRefPubMedGoogle Scholar
  70. Voermans, N. C., Petersson, K. M., Daudey, L., Weber, B., van Spaendonck, K. P., Kremer, H. P. H., & Fernandez, G. (2004). Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron, 43, 427–435.CrossRefPubMedGoogle Scholar
  71. Wais, P. E. (2008). FMRI signals associated with memory strength in the medial temporal lobes: a meta-analysis. Neuropsychologia, 46(14), 3185–3196. doi: 10.1016/j.neuropsychologia.2008.08.025.CrossRefPubMedGoogle Scholar
  72. Wang, L., Zang, Y., He, Y., Liang, M., Zhang, X., Tian, L., & Li, K. (2006). Changes in hippocampal connectivity in the early stages of Alzheimer’s disease: evidence from resting state fMRI. NeuroImage, 31(2), 496–504. doi: 10.1016/j.neuroimage.2005.12.033.CrossRefPubMedGoogle Scholar
  73. Zarahn, E., Rakitin, B., Abela, D., Flynn, J., & Stern, Y. (2007). Age-related changes in brain activation during a delayed item recognition task. Neurobiology of Aging, 28(5), 784–798. doi: 10.1016/j.neurobiolaging.2006.03.002.CrossRefPubMedGoogle Scholar
  74. Zeineh, M. M., Engel, S. A., Thompson, P. M., & Bookheimer, S. Y. (2003). Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science, 299(5606), 577–580. doi: 10.1126/science.1077775.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Christiane S. H. Oedekoven
    • 1
    • 2
  • Andreas Jansen
    • 1
  • James L. Keidel
    • 2
  • Tilo Kircher
    • 1
  • Dirk Leube
    • 1
  1. 1.Department of Psychiatry and PsychotherapyPhilipps-University MarburgMarburgGermany
  2. 2.School of PsychologyUniversity of SussexBrightonUK

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