Experimental Brain Research

, Volume 173, Issue 4, pp 661–672 | Cite as

Precuneus is involved in allocentric spatial location encoding and recognition

  • Lars FringsEmail author
  • Kathrin Wagner
  • Ansgar Quiske
  • Ralf Schwarzwald
  • Joachim Spreer
  • Ulrike Halsband
  • Andreas Schulze-Bonhage
Research Article


Using a declarative memory paradigm, the anatomical correlates of spatial location encoding and retrieval in the healthy human brain as reflected by BOLD fMRI were investigated. During encoding, subjects were instructed to view and keep in mind different locations of an object on a platform seen from different viewpoints in virtual 3D. In retrieval trials, subjects had to recognize previously learned object locations. Comparing activation patterns associated with encoding and recognition on a voxel-by-voxel basis, we found regions in the precuneus bilaterally activated by both processes. To our knowledge, this is the first study that directly compared human brain activation patterns associated with allocentric encoding and retrieval of spatial locations in virtual 3D. Our results provide further information concerning the role of the precuneus in declarative memory processes, pointing to precuneus involvement in encoding and retrieval of spatial locations.


Spatial memory Encoding Retrieval Fmri Precuneus 



We would like to thank Dr. J. Unterrainer for helpful discussion and two anonymous reviewers for valuable suggestions to improve the manuscript.


  1. Aguirre GK, D’Esposito M (1997) Environmental knowledge is subserved by separable dorsal/ventral neural areas. J.Neurosci. 17:2512–2518PubMedGoogle Scholar
  2. Alvarez P, Squire LR (1994) Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci USA 91:7041–7045PubMedCrossRefGoogle Scholar
  3. Astafiev SV, Shulman GL, Stanley CM, Snyder AZ, Van Essen DC, Corbetta M (2003) Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J Neurosci 23:4689–4699PubMedGoogle Scholar
  4. Bernard FA, Bullmore ET, Graham KS, Thompson SA, Hodges JR, Fletcher PC (2004) The hippocampal region is involved in successful recognition of both remote and recent famous faces. Neuroimage 22(4):1704–1714CrossRefPubMedGoogle Scholar
  5. Bohbot VD, Iaria G, Petrides M (2004) Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 18:418–425CrossRefPubMedGoogle Scholar
  6. Buckner RL, Raichle ME, Miezin FM, Petersen SE (1996) Functional anatomic studies of memory retrieval for auditory words and visual pictures. J Neurosci 16:6219–6235PubMedGoogle Scholar
  7. Buckner RL, Wheeler ME (2001) The cognitive neuroscience of remembering. Nat Rev Neurosci 2:624–634CrossRefPubMedGoogle Scholar
  8. Buffalo EA, Bellgowan PSF, Martin A (2004) The hippocampus and the surrounding cortex play different roles in memory. Neuroimage 22Google Scholar
  9. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641CrossRefPubMedGoogle Scholar
  10. Burgess N, Maguire EA, Spiers HJ, O’Keefe J (2001) A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. Neuroimage 14:439–453CrossRefPubMedGoogle Scholar
  11. Burgess PW, Shallice T (1996) Confabulation and the control of recollection. Memory 4:359–411CrossRefPubMedGoogle Scholar
  12. Cabeza R, Dolcos F, Prince SE, Rice HJ, Weissman DH, Nyberg L (2003) Attention-related activity during episodic memory retrieval: a cross-function fMRI study. Neuropsychologia 41:390–399CrossRefPubMedGoogle Scholar
  13. Cabeza R, Nyberg L (2000) Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci 12:1–47PubMedCrossRefGoogle Scholar
  14. Cadoret G, Pike GB, Petrides M (2001) Selective activation of the ventrolateral prefrontal cortex in the human brain during active retrieval processing. Eur J Neurosci 14:1164–1170CrossRefPubMedGoogle Scholar
  15. Cansino S, Maquet P, Dolan RJ, Rugg MD (2002) Brain activity underlying encoding and retrieval of source memory. Cereb Cortex 12:1048–1056CrossRefPubMedGoogle Scholar
  16. Daselaar SM, Veltman DJ, Witter MP (2004) Common pathway in the medial temporal lobe for storage and recovery of words as revealed by event-related functional MRI. Hippocampus 14:163–169CrossRefPubMedGoogle Scholar
  17. Daum I, Ackermann H (1994) Dissociation of declarative and nondeclarative memory after bilateral thalamic lesions: a case report. Int J Neurosci 75:153–165PubMedGoogle Scholar
  18. Dolan RJ, Fletcher PC (1997) Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature 388:582–585CrossRefPubMedGoogle Scholar
  19. Duncan J, Owen AM (2000) Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23:475–483CrossRefPubMedGoogle Scholar
  20. Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601CrossRefPubMedGoogle Scholar
  21. Fletcher PC, Frith CD, Baker SC, Shallice T, Frackowiak RS, Dolan RJ (1995) The mind’s eye–precuneus activation in memory-related imagery. Neuroimage 2:195–200CrossRefPubMedGoogle Scholar
  22. Fletcher PC, Henson RN (2001) Frontal lobes and human memory: insights from functional neuroimaging. Brain 124:849–881CrossRefPubMedGoogle Scholar
  23. Fletcher PC, Henson RNA (2004) Prefrontal cortex and long-term memory encoding and retrieval. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Price CJ, Zeki S, Ashburner J, Penny W (eds) Human brain function. Academic, London, pp 499–514Google Scholar
  24. Friston KJ, Holmes A, Worsley K, Poline J, Frith C, Frackowiak R (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210CrossRefGoogle Scholar
  25. Gabrieli JD, Brewer JB, Desmond JE, Glover GH (1997) Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276:264–266CrossRefPubMedGoogle Scholar
  26. Ghaem O, Mellet E, Crivello F, Tzourio N, Mazoyer B, Berthoz A, Denis M (1997) Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport 8:739–744PubMedGoogle Scholar
  27. 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 124:1841–1854CrossRefPubMedGoogle Scholar
  28. Gorno-Tempini ML, Hutton C, Josephs O, Deichmann R, Price C, Turner R (2002) Echo time dependence of BOLD contrast and susceptibility artifacts. Neuroimage 15:136–142CrossRefPubMedGoogle Scholar
  29. Gould RL, Brown RG, Owen AM, ffytche DH, Howard RJ (2003) fMRI BOLD response to increasing task difficulty during successful paired associates learning. Neuroimage 20:1006–1019CrossRefPubMedGoogle Scholar
  30. Greicius MD, Krasnow B, Boyett-Anderson JM, Eliez S, Schatzberg AF, Reiss AL, Menon V (2003) Regional analysis of hippocampal activation during memory encoding and retrieval: fMRI study. Hippocampus 13:164–174CrossRefPubMedGoogle Scholar
  31. Halsband U, Krause BJ, Schmidt D, Herzog H, Tellmann L, Muller-Gartner HW (1998) Encoding and retrieval in declarative learning: a positron emission tomography study. Behav Brain Res 97:69–78CrossRefPubMedGoogle Scholar
  32. Halsband U, Krause BJ, Sipila H, Teras M, Laihinen A (2002) PET studies on the memory processing of word pairs in bilingual Finnish-English subjects. Behav Brain Res 132:47–57CrossRefPubMedGoogle Scholar
  33. Haxby JV, Grady CL, Horwitz B, Ungerleider LG, Mishkin M, Carson RE, Herscovitch P, Schapiro MB, Rapoport SI (1991) Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc Natl Acad Sci USA 88:1621–1625PubMedCrossRefGoogle Scholar
  34. Heide W, Binkofski F, Seitz RJ, Posse S, Nitschke MF, Freund HJ, Kompf D (2001) Activation of frontoparietal cortices during memorized triple-step sequences of saccadic eye movements: an fMRI study. Eur J Neurosci 13:1177–1189CrossRefPubMedGoogle Scholar
  35. Henson RNA (2004) Explicit memory. In: Frackowiak RS, Friston KJ, Frith CD, Dolan RJ, Price CJ, Zeki S, Ashburner J, Penny W (eds) Human brain function. Academic, London, pp 487–498Google Scholar
  36. Johnsrude IS, Owen AM, Crane J, Milner B, Evans AC (1999) A cognitive activation study of memory for spatial relationships. Neuropsychologia 37:829–841CrossRefPubMedGoogle Scholar
  37. Jordan K, Schadow J, Wuestenberg T, Heinze HJ, Jancke L (2004) Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task. Neuroreport 15:135–140CrossRefPubMedGoogle Scholar
  38. 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 20:927–936CrossRefPubMedGoogle Scholar
  39. Kohler S, Crane J, Milner B (2002) Differential contributions of the parahippocampal place area and the anterior hippocampus to human memory for scenes. Hippocampus 12:718–723CrossRefPubMedGoogle Scholar
  40. Krause BJ, Horwitz B, Taylor JG, Schmidt D, Mottaghy FM, Herzog H, Halsband U, Muller-Gartner H (1999a) Network analysis in episodic encoding and retrieval of word-pair associates: a PET study. Eur J Neurosci 11:3293–3301CrossRefGoogle Scholar
  41. Krause BJ, Schmidt D, Mottaghy FM, Taylor J, Halsband U, Herzog H, Tellmann L, Muller-Gartner HW (1999b) Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. Brain 122(Pt 2):255–263CrossRefGoogle Scholar
  42. Lee AC, Robbins TW, Pickard JD, Owen AM (2000) Asymmetric frontal activation during episodic memory: the effects of stimulus type on encoding and retrieval. Neuropsychologia 38:677–692CrossRefPubMedGoogle Scholar
  43. Lundstrom BN, Petersson KM, Andersson J, Johansson M, Fransson P, Ingvar M (2003) Isolating the retrieval of imagined pictures during episodic memory: activation of the left precuneus and left prefrontal cortex. Neuroimage 20:1934–1943CrossRefPubMedGoogle Scholar
  44. Maguire EA, Frackowiak RS, Frith CD (1997) Recalling routes around london: activation of the right hippocampus in taxi drivers. J Neurosci 17:7103–7110PubMedGoogle Scholar
  45. Maguire EA, Henson RN, Mummery CJ, Frith CD (2001) Activity in prefrontal cortex, not hippocampus, varies parametrically with the increasing remoteness of memories. Neuroreport 12:441–444CrossRefPubMedGoogle Scholar
  46. Mayes AR, Daum I, Markowisch HJ, Sauter B (1997) The relationship between retrograde and anterograde amnesia in patients with typical global amnesia. Cortex 33:197–217PubMedGoogle Scholar
  47. Mazziotta JC, Toga AW, Evans A, Fox P, Lancaster J (1995) A probabilistic atlas of the human brain: theory and rationale for its development. The International Consortium for Brain Mapping (ICBM). Neuroimage 2:89–101CrossRefPubMedGoogle Scholar
  48. McDermott KB, Ojemann JG, Petersen SE, Ollinger JM, Snyder AZ, Akbudak E, Conturo TE, Raichle ME (1999) Direct comparison of episodic encoding and retrieval of words: an event-related fMRI study. Memory 7:661–678CrossRefPubMedGoogle Scholar
  49. Mechelli A, Price CJ, Friston KJ, Ishai A (2004) Where bottom-up meets top-down: neuronal interactions during perception and imagery. Cereb Cortex 14:1256–1265CrossRefPubMedGoogle Scholar
  50. Milner B, Squire LR, Kandel ER (1998) Cognitive neuroscience and the study of memory. Neuron 20:445–468CrossRefPubMedGoogle Scholar
  51. Moscovitch C, Kapur S, Kohler S, Houle S (1995) Distinct neural correlates of visual long-term memory for spatial location and object identity: a positron emission tomography study in humans. Proc Natl Acad Sci USA 92:3721–3725PubMedCrossRefGoogle Scholar
  52. Mottaghy FM, Shah NJ, Krause BJ, Schmidt D, Halsband U, Jancke L, Muller-Gartner HW (1999) Neuronal correlates of encoding and retrieval in episodic memory during a paired-word association learning task: a functional magnetic resonance imaging study. Exp Brain Res 128:332–342CrossRefPubMedGoogle Scholar
  53. Nyberg L, Habib R, McIntosh AR, Tulving E (2000) Reactivation of encoding-related brain activity during memory retrieval. Proc Natl Acad Sci USA 97:11120–11124CrossRefPubMedGoogle Scholar
  54. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. University Press, OxfordGoogle Scholar
  55. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  56. Owen AM (2003) HERA today, gone tomorrow? Trends Cogn Sci 7:383–384CrossRefPubMedGoogle Scholar
  57. Owen AM, Evans AC, Petrides M (1996a) Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. Cereb Cortex 6:31–38Google Scholar
  58. Owen AM, Milner B, Petrides M, Evans AC (1996b) Memory for object features versus memory for object location: a positron-emission tomography study of encoding and retrieval processes. Proc Natl Acad Sci USA 93:9212–9217CrossRefGoogle Scholar
  59. Parslow DM, Rose D, Brooks B, Fleminger S, Gray JA, Giampietro V, Brammer MJ, Williams S, Gasston D, Andrew C, Vythelingum GN, Loannou G, Simmons A, Morris RG (2004) Allocentric spatial memory activation of the hippocampal formation measured with fMRI. Neuropsychology 18(3):450–461CrossRefPubMedGoogle Scholar
  60. Persson J, Nyberg L (2000) Conjunction analysis of cortical activations common to encoding and retrieval. Microsc.Res.Tech. 51:39–44CrossRefPubMedGoogle Scholar
  61. Pihlajamaki M, Tanila H, Kononen M, Hanninen T, Hamalainen A, Soininen H, Aronen HJ (2004) Visual presentation of novel objects and new spatial arrangements of objects differentially activates the medial temporal lobe subareas in humans. Eur J Neurosci 19(7):1939–1949CrossRefPubMedGoogle Scholar
  62. Roland PE, Gulyas B (1995) Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. Cereb Cortex 5:79–93PubMedGoogle Scholar
  63. Schacter DL, Alpert NM, Savage CR, Rauch SL, Albert MS (1996) Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. Proc Natl Acad Sci USA 93:321–325CrossRefPubMedGoogle Scholar
  64. Schmahmann JD, Pandya DN (1997) The cerebrocerebellar system. Int Rev Neurobiol 41:31–60PubMedGoogle Scholar
  65. Schmidt D, Krause BJ, Mottaghy FM, Halsband U, Herzog H, Tellmann L, Muller-Gartner HW (2002) Brain systems engaged in encoding and retrieval of word-pair associates independent of their imagery content or presentation modalities. Neuropsychologia 40:457–470CrossRefPubMedGoogle Scholar
  66. Scoville WB, Milner B (1957). Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatr 20:11–21PubMedCrossRefGoogle Scholar
  67. Shallice T, Fletcher P, Frith CD, Grasby P, Frackowiak RS, Dolan RJ (1994) Brain regions associated with acquisition and retrieval of verbal episodic memory. Nature 368:633–635CrossRefPubMedGoogle Scholar
  68. 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 4:442–449CrossRefPubMedGoogle Scholar
  69. Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci USA 93(24):13515–13522CrossRefPubMedGoogle Scholar
  70. Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380–1386PubMedGoogle Scholar
  71. Stark CE, Squire LR (2001) When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci USA 98:12760–12766PubMedCrossRefGoogle Scholar
  72. Stephan KE, Marshall JC, Friston KJ, Rowe JB, Ritzl A, Zilles K, Fink GR (2003) Lateralized cognitive processes and lateralized task control in the human brain. Science 301:384–386CrossRefPubMedGoogle Scholar
  73. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical, New YorkGoogle Scholar
  74. Tootell RB, Hadjikhani N (2000) Attention—brains at work! Nat Neurosci 3:206–208CrossRefPubMedGoogle Scholar
  75. Tulving E, Kapur S, Craik FI, Moscovitch M, Houle S (1994) Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc Natl Acad Sci USA 91:2016–2020PubMedCrossRefGoogle Scholar
  76. Vaidya CJ, Zhao M, Desmond JE, Gabrieli JD (2002) Evidence for cortical encoding specificity in episodic memory: memory-induced re-activation of picture processing areas. Neuropsychologia 40:2136–2143CrossRefPubMedGoogle Scholar
  77. 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 9:3711–3717PubMedCrossRefGoogle Scholar
  78. 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 14:256–267CrossRefPubMedGoogle Scholar
  79. Wheeler ME, Petersen SE, Buckner RL (2000) Memory’s echo: vivid remembering reactivates sensory-specific cortex. Proc Natl Acad Sci USA 97:11125–11129CrossRefPubMedGoogle Scholar
  80. Zeineh MM, Engel SA, Thompson PM, Bookheimer SY (2003) Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science 299:577–580CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Lars Frings
    • 1
    Email author
  • Kathrin Wagner
    • 1
  • Ansgar Quiske
    • 1
  • Ralf Schwarzwald
    • 2
  • Joachim Spreer
    • 2
  • Ulrike Halsband
    • 3
  • Andreas Schulze-Bonhage
    • 1
  1. 1.Epilepsy CenterUniversity Hospital of FreiburgFreiburgGermany
  2. 2.Department of NeuroradiologyUniversity Hospital of FreiburgFreiburgGermany
  3. 3.Department of Neuropsychology, Institute of PsychologyUniversity of Freiburg FreiburgGermany

Personalised recommendations