Skip to main content
SpringerLink
Log in

Different spatial memory systems are involved in small- and large-scale environments: evidence from patients with temporal lobe epilepsy

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

Abstract

Recent reports show that humans and animals do not acquire information about routes and object locations in the same way. In spatial memory, a specific sub-system is hypothesized to be involved in encoding, storing and recalling navigational information, and it is segregated from the sub-system devoted to small-scale environment. We assessed this hypothesis in a sample of patients treated surgically for intractable temporal lobe epilepsy. We found double dissociations between learning and recall of spatial positions in large space versus small space. These results strongly support the hypothesis that two segregate systems process navigational memory for large-scale environments and spatial memory in small-scale environments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aguirre GK, Detre JA, Alsop DC, D’Esposito M (1996) The parahippocampus subserves topographical learning in man. Cereb Cortex 6:823–829

    Article  CAS  PubMed  Google Scholar 

  • Aguirre GK, Zarahn E, D’Esposito M (1998) An area within human ventral cortex sensitive to “building” stimuli: evidence and implications. Neuron 21:373–383

    Google Scholar 

  • Aimola L, Schindler I, Venneri A (2007) Task-independent neglect in near and far space. A comparison of line bisection and cancellation performance in right brain damaged patients. Neural Plastic 2007:23250

    Google Scholar 

  • Amaral DG, Lavenex P (2007) Hippocampal neuroanatomy. In: Andersen P, Morris R, Amaral DG, Bliss T, O’Keefe J (eds) The hippocampus book. Oxford University Press, Oxford, pp 37–114

    Google Scholar 

  • Berthoz A (1997) Parietal and hippocampal contribution to topokinetic and topographic memory. Phil Trans Royal Soc London Ser B 352:1437–1448

    Article  CAS  Google Scholar 

  • Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9(3):182–194

    Google Scholar 

  • Bisiach E, Perani D, Vallar G, Berti A (1986) Unilateral neglect: personal and extrapersonal. Neuropsychol 24:759–767

    Article  CAS  Google Scholar 

  • Bohbot VD, Kalina M, Stepankova K, Spackova N, Petrides M, Nadel L (1998) Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychol 36:1217–1238

    Google Scholar 

  • Burguière E, Arleo A, Hojjati MR, Elgersma Y, De Zeeuw CI, Berthoz A, Rondi-Reig L (2005) Spatial navigation impairment in mice lacking cerebellar LTD: a motor adaptation deficit? Nat Neurosci 8(10):1292–1294

    Article  PubMed  Google Scholar 

  • Cavazzuti V, Winston K, Baker P, Welsh K (1980) Psychological changes following surgery for tumours in the temporal lobe. J Neurosurg 53:618–626

    Article  CAS  PubMed  Google Scholar 

  • Committeri G, Galati G, Paradis A-L, Pizzamiglio L, Berthoz A, Lebihan D (2004) Frames for spatial cognition: different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location. J Cognitive Neurosci 16(9):1517–1535

    Article  Google Scholar 

  • Committeri G, Pitzalis S, Galati G, Patria F, Pelle G, Sabatini U, Castriota-Scanderbeg A, Piccardi L, Guariglia C, Pizzamiglio L (2007) Neural bases of personal and extrapersonal neglect in humans. Brain 130:431–441

    Article  PubMed  Google Scholar 

  • Corsi PM (1975) Human memory and the medial temporal region of the brain, Dissertation Abstracts International, 34(02)(1972), 891B (University micro-lms No. AA105-77717)

  • Crawford JR, Garthwaite PH (2007) Comparison of a single case to a control or normative sample in neuropsychology: development of a Bayesan approach. Cognitive Neuropsychol 24(4):343–372

    Article  Google Scholar 

  • Crawford JR, Howell DC (1998) Comparing an individual’s test score against norms derived from small samples. Clin Neuropsychol 12:482–486

    Google Scholar 

  • Dupont S, Duron E, Samson S, Volle E, Delmaire C, Denos M, Navarro V, Chiras J, Lehéricy S, Baulac M (2010) fMRI or WADA test: which is the better predictor of individual postoperative memory outcome? Radiology 255(1):128–134

    Google Scholar 

  • Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory [Review]. Annu Rev Neurosci 30:123–152

    Google Scholar 

  • Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature 425:184–188

    Article  CAS  PubMed  Google Scholar 

  • Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601

    Google Scholar 

  • Falconer MA (1971) Anterior temporal lobectomy for epilepsy. In: Rob C, Smith R (eds) Operative surgery. Butterworths, London, pp 142–149

    Google Scholar 

  • 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 8:739–744

    Article  CAS  PubMed  Google Scholar 

  • Guariglia C, Antonucci G (1992) Personal and extrapersonal space: a case of neglect dissociation. Neuropsychol 30:1001–1009

    Article  CAS  Google Scholar 

  • Habib M, Sirigu A (1987) Pure topographical disorientation: a definition and anatomical basis. Cortex 23:73–85

    Google Scholar 

  • Halligan PW, Marshall JC (1991) Left neglect for near but not far space in man. Nature 350:498–500

    Article  CAS  PubMed  Google Scholar 

  • Hartley T, Burgess N (2005) Complementary memory systems: competition, cooperation and compensation. Trends Neurosci 28(4):169–170

    Article  CAS  PubMed  Google Scholar 

  • Hartley T, Maguire EA, Spiers HJ, Burgess N (2003) The well-worn route and the path less travelled: distinct neural bases of route following and wayfinding in humans. Neuron 37(5):877–888

    Article  CAS  PubMed  Google Scholar 

  • Hermann BP, Wyler AR, Bush AJ, Tabatabai FR (1992) Differential effects of left and right anterior temporal lobectomy on verbal learning and memory performance. Epilepsia 33(2):289–297

    Article  CAS  PubMed  Google Scholar 

  • Hermann BP, Seidenberg M, Haltiner A, Wyler AR (1995) Relationship of age at onset, chronologic age and adequacy of preoperative performance to verbal memory change after anterior temporal lobectomy. Epilepsia 36(2):137–145

    Google Scholar 

  • Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD (2003) Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J Neurosci 23(13):5945–5952

    Google Scholar 

  • Incisa della Rocchetta A, Samson S, Ehrlé N, Denos M, Hasboun D, Baulac M (2004) Memory for visuospatial location following selective hippocampal sclerosis: the use of different co-ordinate systems. Neuropsychol 18:15–28

    Article  CAS  Google Scholar 

  • Insausti R, Amaral DG (2004) Hippocampal formation. In: Paxinos G, Mai J (eds) The human nervous system. Elsevier, Amsterdam, pp 871–915

    Chapter  Google Scholar 

  • Ivnik RJ, Sharbrough FW, Laws ER (1987) Effects of anterior temporal lobectomy on cognitive function. J Clin Psychol 43:128–137

    Article  CAS  PubMed  Google Scholar 

  • Kessels RPC, de Haan EHF, Kappelle LJ, Postma A (2001) Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions. Brain Res Rev 35:295–303

    Article  CAS  PubMed  Google Scholar 

  • Lambrey S, Samson S, Dupont S, Baulac M, Berthoz A (2003) Reference frames and cognitive strategies during navigation: is the left hippocampal formation involved in the sequential aspects of route memory? Int Congress Ser 1250:261–274

    Article  Google Scholar 

  • Lambrey S, Amorin M-A, Samson S, Noulhiane M, Hasboun D, Dupont S, Baulac M, Berthoz A (2008) Distinct visual perspective-taking strategies involve the left and right medial temporal lobe structures differently. Brain 131:523–534

    Article  CAS  PubMed  Google Scholar 

  • Maguire E, Burke T, Phillips J, Staunton H (1996) Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychol 34:993–1001

    Google Scholar 

  • Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J (1998) Knowing where and getting there: a human navigation network. Science 280:921–924

    Article  CAS  PubMed  Google Scholar 

  • Marangolo P, Piccardi L, Rinaldi MC (2003) Dissociation between personal and extrapersonal neglect in a crossed aphasia study. Neurocase 9:414–420

    Article  PubMed  Google Scholar 

  • Mellet E, Briscogne S, Tzourio-Mazoyer N, Ghaem O, Petit L, Zago L, Etard O, Berthoz A, Mazoyer B, Denis M (2000) Neural correlates of topographic mental exploration: the impact of route versus survey perspective learning. Neuroimage 12:588–600

    Article  CAS  PubMed  Google Scholar 

  • Morris R (2007) Theories of hippocampal function. In: Andersen P, Morris R, Amaral DG, Bliss T, O’Keefe J (eds) The hippocampus book. Oxford University Press, Oxford, pp 581–713

  • Murray EA, Bussey TJ, Saksida LM (2007) Visual perception and memory: a new view of medial temporal lobe function in primates and rodents [Review]. Annu Rev Neurosci 30:99–122

    Google Scholar 

  • Ojemann GA, Dodrill CB (1985) Verbal memory impairments after temporal lobectomy for epilepsy. J Neurosurg 62:101–107

    Article  CAS  PubMed  Google Scholar 

  • Peru A, Pinna G (1997) Right personal neglect following a left hemisphere stroke: a case report. Cortex 33:585–590

    Article  CAS  PubMed  Google Scholar 

  • Piccardi L, Iaria G, Ricci M, Bianchini F, Zompanti L, Guariglia C (2008) Walking in the Corsi test: which type of memory do you need? Neurosci Lett 432:127–131

    Article  CAS  PubMed  Google Scholar 

  • Pigott S, Milner B (1993) Memory for different aspects of complex visual scenes after unilateral temporal or frontal lobe resection. Neuropsychol 31(1):1–15

    Google Scholar 

  • Schmidt D, Krause BJ, Weiss PH et al (2007) Visuospatial working memory and changes of the point of view in 3D space. Neuroimage 36:955–968

    Article  CAS  PubMed  Google Scholar 

  • Scoville WB (1954) The limbic lobe in man. J Neurosurg 11:64–66

    Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psych 20:11–21

    Google Scholar 

  • Smith ML, Milner B (1989) Right hippocampal impairment in the recall of spatial location: encoding deficit or rapid forgetting? Neuropsychol 27:71–81

    Google Scholar 

  • Spinnler H, Tognoni G (1987) Standardizzazione e taratura italiana di test neuropsicologici. Ital J Neurol Sci 8:1–120

    Google Scholar 

  • Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe [Review]. Annu Rev Neurosci 27:279–306

    Google Scholar 

  • Voermans NC, Petersson KM, Daudey L, Weber B, van Spaendonck KP, Kremer HPH, Fernández G (2004) Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 43:427–435

    Google Scholar 

  • Vuilleumier P, Valenza N, Mayer E, Reverdin A, Landis T (1998) Near and far visual space in unilateral neglect. Ann Neurol 43:406–410

    Article  CAS  PubMed  Google Scholar 

  • Wada J, Rasmussen T (1960) Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. J Neurosurg 17:266–282

    Article  Google Scholar 

  • White NM, McDonald RJ (2002) Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77:125–184

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by grants to C.G. and to A.B. from the European Community (FP6-NEST: Wayfinding, 12959).

Author information

Authors and Affiliations

  1. Dipartimento di Scienze della Salute, Università degli Studi dell’Aquila, Via Vetoio, 67100, Coppito 2 (AQ), Italy

    L. Piccardi

  2. Cenro Ricerche di Neuropsicologia, I.R.C.C.S. Fondazione Santa Lucia, Via Ardeatina 306, 00179, Rome, Italy

    L. Piccardi & C. Guariglia

  3. Unité d’épilepsie, Groupe Hospitalier Pitié Salpêtrière, 45 Bd de l’Hôpital, 75651, Paris cedex 13, France

    M. Baulac, M. Denos, S. Dupont & S. Samson

  4. LPPA, College de France, Paris, France

    A. Berthoz

  5. Dipartimento Psicologia 39, Sapienza Università di Roma, Via Dei Marsi 78, 00185, Rome, Italy

    C. Guariglia

  6. CNRS 8160, Université Lille, Nord de France, Lille, France

    S. Samson

Authors
  1. L. Piccardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Berthoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Baulac
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Denos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Dupont
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Samson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C. Guariglia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Piccardi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Piccardi, L., Berthoz, A., Baulac, M. et al. Different spatial memory systems are involved in small- and large-scale environments: evidence from patients with temporal lobe epilepsy. Exp Brain Res 206, 171–177 (2010). https://doi.org/10.1007/s00221-010-2234-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-010-2234-2

Keywords

Search

Navigation