Anterior hippocampus orchestrates successful encoding and retrieval of non-relational memory: an event-related fMRI study

  • Tilo Kircher
  • Susanne Weis
  • Dirk Leube
  • Katrin Freymann
  • Michael Erb
  • Frank Jessen
  • Wolfgang Grodd
  • Reinhard Heun
  • Sören Krach
ORIGINAL PAPER

Abstract

Episodic memory encoding and retrieval processes have been linked to different neural networks. However, the common brain regions associated with non-relational memory processing during successful encoding (subsequent memory effect) and successful retrieval (recognition effect) have not yet been investigated. Further, the majority of functional imaging studies have been conducted in young subjects, whereas patients from lesion studies, where most neuropsychological models are still based upon, are usually older. Inferences from younger subjects cannot necessarily be applied to the elderly, an issue becoming particularly relevant with our ageing society. Using an event-related fMRI approach we studied 29 healthy elderly subjects (mean age 67.8, SD 5.4 years) with a non-associative task of intentional word list encoding and retrieval. For each subject, behavioural responses were individually classified into four event types (hits test, misses test, false alarms, correct rejections). Brain areas activated during successful memory encoding comprised the anterior left hippocampus extending into the surrounding parahippocampal gyrus. Regions associated with successful memory retrieval involved a wide-spread network of anterior left parahippocampal gyrus, bilateral temporal cortices and bilateral ventral and dorsal prefrontal areas. Regions contributing to both successful encoding and retrieval, evidenced by a conjunction analysis, revealed prominent left lateralized activations of the anterior hippocampus and the inferior parietal lobe. Our results indicate that the anterior left hippocampus plays an important role during successful memory encoding and during successful memory retrieval in a task of simple, non-associative wordlist learning in healthy elderly subjects.

Keywords

non-relational memory hippocampus er-fMRI 

Notes

Acknowledgments

The study was supported by grants from the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG Nr. HE 2318/4-1 and GR 833/7-1) and by a grant from the Interdisciplinary Center for Clinical Research “BIOMAT.” within the Faculty of Medicine at the RWTH Aachen University (IZKF VV N68).

References

  1. 1.
    Baschek IL, Bredenkamp J, Oehrle B, Wippich W (1977) Bestimmung der Bildhaftigkeit (I), Konkretheit (C) und der Bedeutungshaltigkeit (m’) von 800 Substantiven [The determination of imagery (i), concreteness (c), and meaningfulness of 800 nouns]. Zeitschrift für experimentelle und angewandte Psychologie 25:353–396Google Scholar
  2. 2.
    Brassen S, Weber-Fahr W, Sommer T, Lehmbeck JT, Braus DF (2006) Hippocampal–prefrontal encoding activation predicts whether words can be successfully recalled or only recognized. Behav Brain Res 171(2):271–278PubMedCrossRefGoogle Scholar
  3. 3.
    Braver TS, Barch DM, Kelley WM, Buckner RL, Cohen NJ, Miezin FM, Snyder AZ, Ollinger JM, Akbudak E, Conturo TE, Petersen SE (2001) Direct comparison of prefrontal cortex regions engaged by working and long-term memory tasks. Neuroimage 14(1 Pt 1):48–59PubMedCrossRefGoogle Scholar
  4. 4.
    Brewer JB, Zhao Z, Desmond JE, Glover GH, Gabrieli JD (1998) Making memories: brain activity that predicts how well visual experience will be remembered. Science 281(5380):1185–1187PubMedCrossRefGoogle Scholar
  5. 5.
    Buckner RL, Koutstaal W, Schacter DL, Wagner AD, Rosen BR (1998) Functional-anatomic study of episodic retrieval using fMRI. I. Retrieval effort versus retrieval success. Neuroimage 7(3):151–162PubMedCrossRefGoogle Scholar
  6. 6.
    Buckner RL, Raichle ME, Miezin FM, Petersen SE (1996) Functional anatomic studies of memory retrieval for auditory words and visual pictures. J Neurosci 16(19):6219–6235PubMedGoogle Scholar
  7. 7.
    Cabeza R (2002) Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol Aging 17(1):85–100PubMedCrossRefGoogle Scholar
  8. 8.
    Cabeza R, Anderson ND, Locantore JK, McIntosh AR (2002) Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17(3):1394–1402PubMedCrossRefGoogle Scholar
  9. 9.
    Cabeza R, Grady CL, Nyberg L, McIntosh AR, Tulving E, Kapur S, Jennings JM, Houle S, Craik FI (1997) Age-related differences in neural activity during memory encoding and retrieval: a positron emission tomography study. J Neurosci 17(1):391–400PubMedGoogle Scholar
  10. 10.
    Daselaar SM, Veltman DJ, Rombouts SA, Raaijmakers JG, Jonker C (2003) Deep processing activates the medial temporal lobe in young but not in old adults. Neurobiol Aging 24(7):1005–1011PubMedCrossRefGoogle Scholar
  11. 11.
    Davachi L, Mitchell JP, Wagner AD (2003) Multiple routes to memory: distinct medial temporal lobe processes build item and source memories. Proc Natl Acad Sci USA 100(4):2157–2162PubMedCrossRefGoogle Scholar
  12. 12.
    Dolan RJ, Fletcher PF (1999) Encoding and retrieval in human medial temporal lobes: an empirical investigation using functional magnetic resonance imaging (fMRI). Hippocampus 9(1):25–34PubMedCrossRefGoogle Scholar
  13. 13.
    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(3):189–198PubMedCrossRefGoogle Scholar
  14. 14.
    Friston KJ, Penny WD, Glaser DE (2005) Conjunction revisited. Neuroimage 25(3):661–667PubMedCrossRefGoogle Scholar
  15. 15.
    Giovanello KS, Schnyer DM, Verfaellie M (2004) A critical role for the anterior hippocampus in relational memory: evidence from an fMRI study comparing associative and item recognition. Hippocampus 14(1):5–8PubMedCrossRefGoogle Scholar
  16. 16.
    Giovanello KS, Verfaellie M, Keane MM (2003) Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cogn Affect Behav Neurosci 3(3):186–194PubMedCrossRefGoogle Scholar
  17. 17.
    Golby AJ, Poldrack RA, Brewer JB, Spencer D, Desmond JE, Aron AP, Gabrieli JD (2001) Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain 124(Pt 9):1841–1884PubMedCrossRefGoogle Scholar
  18. 18.
    Gold JJ, Hopkins RO, Squire LR (2006) Single-item memory, associative memory, and the human hippocampus. Learn Mem 13(5):644–649PubMedCrossRefGoogle Scholar
  19. 19.
    Grady CL, McIntosh AR, Horwitz B, Maisog JM, Ungerleider LG, Mentis MJ, Pietrini P, Schapiro MB, Haxby JV (1995) Age-related reductions in human recognition memory due to impaired encoding. Science 269(5221):218–221PubMedCrossRefGoogle Scholar
  20. 20.
    Helmstaedter C, Lendt M, Lux S (2001) Verbaler Lern- und Merkfähigkeitstest (VLMT), Göttingen: HogrefeGoogle Scholar
  21. 21.
    Henke K, Buck A, Weber B, Wieser HG (1997) Human hippocampus establishes associations in memory. Hippocampus 7(3):249–256PubMedCrossRefGoogle Scholar
  22. 22.
    Iidaka T, Sadato N, Yamada H, Yonekura Y (2000) Functional asymmetry of human prefrontal cortex in verbal and non-verbal episodic memory as revealed by fMRI. Brain Res Cogn Brain Res 9(1):73–83PubMedCrossRefGoogle Scholar
  23. 23.
    Kelley WM, Miezin FM, McDermott KB, Buckner RL, Raichle ME, Cohen NJ, Ollinger JM, Akbudak E, Conturo TE, Snyder AZ, Petersen SE (1998) Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron 20(5):927–936PubMedCrossRefGoogle Scholar
  24. 24.
    Kircher T, Weis S, Freymann K, Erb M, Jessen F, Grodd W, Heun R, Leube DT (2007) Hippocampal activation in MCI patients is necessary for successful memory encoding. J Neurol Neurosurg PsychiatryGoogle Scholar
  25. 25.
    Kirchhoff BA, Wagner AD, Maril A, Stern CE (2000) Prefrontal–temporal circuitry for episodic encoding and subsequent memory. J Neurosci 20(16):6173–6180PubMedGoogle Scholar
  26. 26.
    Konishi S, Wheeler ME, Donaldson DI, Buckner RL (2000) Neural correlates of episodic retrieval success. Neuroimage 12(3):276–286PubMedCrossRefGoogle Scholar
  27. 27.
    Lepage M, Habib R, Tulving E (1998) Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus 8(4):313–322PubMedCrossRefGoogle Scholar
  28. 28.
    Leube DT, Erb M, Grodd W, Bartels M, Kircher TT (2003) Successful episodic memory retrieval of newly learned faces activates a left fronto-parietal network. Brain Res Cogn Brain Res 18(1):97–101PubMedCrossRefGoogle Scholar
  29. 29.
    McDermott KB, Buckner RL, Petersen SE, Kelley WM, Sanders AL (1999) Set- and code-specific activation in frontal cortex: an fMRI study of encoding and retrieval of faces and words. J Cogn Neurosci 11(6):631–640PubMedCrossRefGoogle Scholar
  30. 30.
    Milner B, Johnsrude I, Crane J (1997) Right medial temporal-lobe contribution to object-location memory. Philos Trans R Soc Lond B Biol Sci 352(1360):1469–1474PubMedCrossRefGoogle Scholar
  31. 31.
    Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25(3):653–660PubMedCrossRefGoogle Scholar
  32. 32.
    Nyberg L, McIntosh AR, Houle S, Nilsson LG, Tulving E (1996) Activation of medial temporal structures during episodic memory retrieval. Nature 380(6576):715–717PubMedCrossRefGoogle Scholar
  33. 33.
    Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113PubMedCrossRefGoogle Scholar
  34. 34.
    Oldigs-Kerber J, Adamus WS, Kitzinger M (1991) Zur Beeinflussung von verbalen Lern- und Gedächtnisprozessen durch Anticholinergica am Beispiel von Scopolamin. Ein pharmakopsychologischer Beitrag für die neuropsychologische Praxis [The impact of anticholinergic drugs on verbal encoding and retrieval processes considering as example scopolamine. A pharmacopsychological contribution for the neuropsychological practice]. Zeitschrift für Neuropsychologie 2:29–40Google Scholar
  35. 35.
    Prince SE, Daselaar SM, Cabeza R (2005) Neural correlates of relational memory: successful encoding and retrieval of semantic and perceptual associations. J Neurosci 25(5):1203–1210PubMedCrossRefGoogle Scholar
  36. 36.
    Ranganath C, Heller A, Cohen MX, Brozinsky CJ, Rissman J (2005) Functional connectivity with the hippocampus during successful memory formation. Hippocampus 15(8):997–1005PubMedCrossRefGoogle Scholar
  37. 37.
    Rypma B, D’Esposito M (2003) A subsequent-memory effect in dorsolateral prefrontal cortex. Brain Res Cogn Brain Res 16(2):162–166PubMedCrossRefGoogle Scholar
  38. 38.
    Saykin AJ, Johnson SC, Flashman LA, McAllister TW, Sparling M, Darcey TM, Moritz CH, Guerin SJ, Weaver J, Mamourian A (1999) Functional differentiation of medial temporal and frontal regions involved in processing novel and familiar words: an fMRI study. Brain 122(Pt 10):1963–1971PubMedCrossRefGoogle Scholar
  39. 39.
    Schacter DL, Wagner AD (1999) Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 9(1):7–24PubMedCrossRefGoogle Scholar
  40. 40.
    Small SA, Nava AS, Perera GM, DeLaPaz R, Mayeux R, Stern Y (2001) Circuit mechanisms underlying memory encoding and retrieval in the long axis of the hippocampal formation. Nat Neurosci 4(4):442–449PubMedCrossRefGoogle Scholar
  41. 41.
    Sperling R, Chua E, Cocchiarella A, Rand-Giovannetti E, Poldrack R, Schacter DL, Albert M (2003) Putting names to faces: successful encoding of associative memories activates the anterior hippocampal formation. Neuroimage 20(2):1400–1410PubMedCrossRefGoogle Scholar
  42. 42.
    Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253(5026):1380–1386PubMedCrossRefGoogle Scholar
  43. 43.
    Stark CE, Squire LR (2003) Hippocampal damage equally impairs memory for single items and memory for conjunctions. Hippocampus 13(2):281–292PubMedCrossRefGoogle Scholar
  44. 44.
    Stark CE, Squire LR (2001) Simple and associative recognition memory in the hippocampal region. Learn Mem 8(4):190–197PubMedCrossRefGoogle Scholar
  45. 45.
    Strange BA, Hurlemann R, Duggins A, Heinze HJ, Dolan RJ (2005) Dissociating intentional learning from relative novelty responses in the medial temporal lobe. Neuroimage 25(1):51–62PubMedCrossRefGoogle Scholar
  46. 46.
    Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Stuttgart, Germany: ThiemeGoogle Scholar
  47. 47.
    Tendolkar I, Arnold J, Petersson KM, Weis S, Anke B-D, van Eijndhoven P, Buitelaar J, Fernandez G (2007) Probing the neural correlates of associative memory formation: a parametrically analyzed event-related functional MRI study. Brain ResGoogle Scholar
  48. 48.
    Tulving E (1983) Elements of episodic memory. Clarendon Press, OxfordGoogle Scholar
  49. 49.
    van der Veen FM, Nijhuis FA, Tisserand DJ, Backes WH, Jolles J (2006) Effects of aging on recognition of intentionally and incidentally stored words: an fMRI study. Neuropsychologia 44(12):2477–2486PubMedCrossRefGoogle Scholar
  50. 50.
    Vargha-Khadem F, Gadian DG, Watkins KE, Connelly A, Van Paesschen W, Mishkin M (1997) Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277(5324):376–380PubMedCrossRefGoogle Scholar
  51. 51.
    Wagner AD, Poldrack RA, Eldridge LL, Desmond JE, Glover GH, Gabrieli JD (1998) Material-specific lateralization of prefrontal activation during episodic encoding and retrieval. Neuroreport 9(16):3711–3717PubMedCrossRefGoogle Scholar
  52. 52.
    Wagner AD, Schacter DL, Rotte M, Koutstaal W, Maril A, Dale AM, Rosen BR, Buckner RL (1998) Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281(5380):1188–1191PubMedCrossRefGoogle Scholar
  53. 53.
    Weis S, Klaver P, Reul J, Elger CE, Fernandez G (2004) Temporal and cerebellar brain regions that support both declarative memory formation and retrieval. Cereb Cortex 14(3):256–267PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Tilo Kircher
    • 1
  • Susanne Weis
    • 2
  • Dirk Leube
    • 1
  • Katrin Freymann
    • 3
  • Michael Erb
    • 4
  • Frank Jessen
    • 3
  • Wolfgang Grodd
    • 4
  • Reinhard Heun
    • 5
  • Sören Krach
    • 1
    • 6
  1. 1.Department of PsychiatryRWTH Aachen University HospitalAachenGermany
  2. 2.Department of NeurologyRWTH Aachen University HospitalAachenGermany
  3. 3.Department of PsychiatryUniversity of BonnBonnGermany
  4. 4.Section of Experimental Magnetic Resonance of CNS, Department of NeuroradiologyUniversity of TuebingenTuebingenGermany
  5. 5.Department of PsychiatryUniversity of BirminghamBirminghamUK
  6. 6.Central Service Facility “Functional Imaging” at the ICCR-BiomatRWTH Aachen University HospitalAachenGermany

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