Skip to main content
Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 2003 Jan;74(1):61–69. doi: 10.1136/jnnp.74.1.61

Loss of spatial learning in a patient with topographical disorientation in new environments

P Turriziani 1, G Carlesimo 1, R Perri 1, F Tomaiuolo 1, C Caltagirone 1
PMCID: PMC1738197  PMID: 12486268

Abstract

The case is described of a patient who, following cerebral hypoxia, developed severe difficulty in orienting himself in new environments in the context of a mild global amnesic syndrome. Some episodes he related suggested that his main difficulty was remembering the spatial/directional value of landmarks he recognised. A neuroradiological examination documented severe bilateral atrophy of the hippocampi associated with atrophic changes in the cerebral hemispheres, most marked in the dorsal regions. Neuropsychological and experimental evaluation showed a severe deficit of spatial learning with substantially preserved ability to learn verbal and visual-object information. He was also virtually unable to learn a route in a maze task based exclusively on spatial data, but the availability of visual cues substantially improved his learning. Finally, he performed within normal limits on various tests investigating knowledge acquired premorbidly regarding famous buildings, routes in the town he had been living in since childhood, and geography. Topographical disorientation may be subtended by a specific difficulty in storing the spatial/directional value of visual landmarks in novel environments. The hippocampus appears to be involved in the acquisition of new topographical spatial knowledge.

Full Text

The Full Text of this article is available as a PDF (196.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguirre G. K., D'Esposito M. Environmental knowledge is subserved by separable dorsal/ventral neural areas. J Neurosci. 1997 Apr 1;17(7):2512–2518. doi: 10.1523/JNEUROSCI.17-07-02512.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aguirre G. K., D'Esposito M. Topographical disorientation: a synthesis and taxonomy. Brain. 1999 Sep;122(Pt 9):1613–1628. doi: 10.1093/brain/122.9.1613. [DOI] [PubMed] [Google Scholar]
  3. Aguirre G. K., Detre J. A., Alsop D. C., D'Esposito M. The parahippocampus subserves topographical learning in man. Cereb Cortex. 1996 Nov-Dec;6(6):823–829. doi: 10.1093/cercor/6.6.823. [DOI] [PubMed] [Google Scholar]
  4. Aguirre G. K., Zarahn E., D'Esposito M. Neural components of topographical representation. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):839–846. doi: 10.1073/pnas.95.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barnes C. A. Spatial learning and memory processes: the search for their neurobiological mechanisms in the rat. Trends Neurosci. 1988 Apr;11(4):163–169. doi: 10.1016/0166-2236(88)90143-9. [DOI] [PubMed] [Google Scholar]
  6. Barrash J., Damasio H., Adolphs R., Tranel D. The neuroanatomical correlates of route learning impairment. Neuropsychologia. 2000;38(6):820–836. doi: 10.1016/s0028-3932(99)00131-1. [DOI] [PubMed] [Google Scholar]
  7. Benton A. L., Varney N. R., Hamsher K. D. Visuospatial judgment. A clinical test. Arch Neurol. 1978 Jun;35(6):364–367. doi: 10.1001/archneur.1978.00500300038006. [DOI] [PubMed] [Google Scholar]
  8. Bottini G., Cappa S., Geminiani G., Sterzi R. Topographic disorientation--a case report. Neuropsychologia. 1990;28(3):309–312. doi: 10.1016/0028-3932(90)90024-i. [DOI] [PubMed] [Google Scholar]
  9. Brooks L. R. The suppression of visualization by reading. Q J Exp Psychol. 1967 Nov;19(4):289–299. doi: 10.1080/14640746708400105. [DOI] [PubMed] [Google Scholar]
  10. Cammalleri R., Gangitano M., D'Amelio M., Raieli V., Raimondo D., Camarda R. Transient topographical amnesia and cingulate cortex damage: a case report. Neuropsychologia. 1996 Apr;34(4):321–326. doi: 10.1016/0028-3932(95)00108-5. [DOI] [PubMed] [Google Scholar]
  11. Carlesimo G. A., Caltagirone C., Gainotti G. The Mental Deterioration Battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The Group for the Standardization of the Mental Deterioration Battery. Eur Neurol. 1996;36(6):378–384. doi: 10.1159/000117297. [DOI] [PubMed] [Google Scholar]
  12. Carlesimo G. A., Fadda L., Turriziani P., Tomaiuolo F., Caltagirone C. Selective sparing of face learning in a global amnesic patient. J Neurol Neurosurg Psychiatry. 2001 Sep;71(3):340–346. doi: 10.1136/jnnp.71.3.340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Carlesimo G. A., Perri R., Turriziani P., Tomaiuolo F., Caltagirone C. Remembering what but not where: independence of spatial and visual working memory in the human brain. Cortex. 2001 Sep;37(4):519–534. doi: 10.1016/s0010-9452(08)70591-4. [DOI] [PubMed] [Google Scholar]
  14. Cave C. B., Squire L. R. Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus. Hippocampus. 1991 Jul;1(3):329–340. doi: 10.1002/hipo.450010323. [DOI] [PubMed] [Google Scholar]
  15. Chalfonte B. L., Verfaellie M., Johnson M. K., Reiss L. Spatial location memory in amnesia: binding item and location information under incidental and intentional encoding conditions. Memory. 1996 Nov;4(6):591–614. doi: 10.1080/741940998. [DOI] [PubMed] [Google Scholar]
  16. Cipolotti L., Robinson G., Blair J., Frith U. Fractionation of visual memory: evidence from a case with multiple neurodevelopmental impairments. Neuropsychologia. 1999 Apr;37(4):455–465. doi: 10.1016/s0028-3932(98)00086-4. [DOI] [PubMed] [Google Scholar]
  17. De Renzi E., Faglioni P., Villa P. Topographical amnesia. J Neurol Neurosurg Psychiatry. 1977 May;40(5):498–505. doi: 10.1136/jnnp.40.5.498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Grön G., Wunderlich A. P., Spitzer M., Tomczak R., Riepe M. W. Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat Neurosci. 2000 Apr;3(4):404–408. doi: 10.1038/73980. [DOI] [PubMed] [Google Scholar]
  19. Habib M., Sirigu A. Pure topographical disorientation: a definition and anatomical basis. Cortex. 1987 Mar;23(1):73–85. doi: 10.1016/s0010-9452(87)80020-5. [DOI] [PubMed] [Google Scholar]
  20. Hanley J. R., Pearson N. A., Young A. W. Impaired memory for new visual forms. Brain. 1990 Aug;113(Pt 4):1131–1148. doi: 10.1093/brain/113.4.1131. [DOI] [PubMed] [Google Scholar]
  21. Hublet C., Demeurisse G. Pure topographical disorientation due to a deep-seated lesion with cortical remote effects. Cortex. 1992 Mar;28(1):123–128. doi: 10.1016/s0010-9452(13)80170-0. [DOI] [PubMed] [Google Scholar]
  22. Hécaen H., Tzortzis C., Rondot P. Loss of topographic memory with learning deficits. Cortex. 1980 Dec;16(4):525–542. doi: 10.1016/s0010-9452(80)80001-3. [DOI] [PubMed] [Google Scholar]
  23. Kapur N. Syndromes of retrograde amnesia: a conceptual and empirical synthesis. Psychol Bull. 1999 Nov;125(6):800–825. doi: 10.1037/0033-2909.125.6.800. [DOI] [PubMed] [Google Scholar]
  24. Landis T., Cummings J. L., Benson D. F., Palmer E. P. Loss of topographic familiarity. An environmental agnosia. Arch Neurol. 1986 Feb;43(2):132–136. doi: 10.1001/archneur.1986.00520020026011. [DOI] [PubMed] [Google Scholar]
  25. Landis T., Cummings J. L., Benson D. F., Palmer E. P. Loss of topographic familiarity. An environmental agnosia. Arch Neurol. 1986 Feb;43(2):132–136. doi: 10.1001/archneur.1986.00520020026011. [DOI] [PubMed] [Google Scholar]
  26. Levine D. N., Warach J., Farah M. Two visual systems in mental imagery: dissociation of "what" and "where" in imagery disorders due to bilateral posterior cerebral lesions. Neurology. 1985 Jul;35(7):1010–1018. doi: 10.1212/wnl.35.7.1010. [DOI] [PubMed] [Google Scholar]
  27. Maguire E. A., Burgess N., Donnett J. G., Frackowiak R. S., Frith C. D., O'Keefe J. Knowing where and getting there: a human navigation network. Science. 1998 May 8;280(5365):921–924. doi: 10.1126/science.280.5365.921. [DOI] [PubMed] [Google Scholar]
  28. Maguire E. A., Burke T., Phillips J., Staunton H. Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia. 1996 Oct;34(10):993–1001. doi: 10.1016/0028-3932(96)00022-x. [DOI] [PubMed] [Google Scholar]
  29. Maguire E. A., Cipolotti L. Selective sparing of topographical memory. J Neurol Neurosurg Psychiatry. 1998 Dec;65(6):903–909. doi: 10.1136/jnnp.65.6.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Maguire E. A., Frackowiak R. S., Frith C. D. Learning to find your way: a role for the human hippocampal formation. Proc Biol Sci. 1996 Dec 22;263(1377):1745–1750. doi: 10.1098/rspb.1996.0255. [DOI] [PubMed] [Google Scholar]
  31. Maguire E. A., Frackowiak R. S., Frith C. D. Recalling routes around london: activation of the right hippocampus in taxi drivers. J Neurosci. 1997 Sep 15;17(18):7103–7110. doi: 10.1523/JNEUROSCI.17-18-07103.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Maguire E. A., Frith C. D., Burgess N., Donnett J. G., O'Keefe J. Knowing where things are parahippocampal involvement in encoding object locations in virtual large-scale space. J Cogn Neurosci. 1998 Jan;10(1):61–76. doi: 10.1162/089892998563789. [DOI] [PubMed] [Google Scholar]
  33. Maguire E. A., Frith C. D., Cipolotti L. Distinct neural systems for the encoding and recognition of topography and faces. Neuroimage. 2001 Apr;13(4):743–750. doi: 10.1006/nimg.2000.0712. [DOI] [PubMed] [Google Scholar]
  34. Maguire E. A., Gadian D. G., Johnsrude I. S., Good C. D., Ashburner J., Frackowiak R. S., Frith C. D. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4398–4403. doi: 10.1073/pnas.070039597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mayes A. R., Meudell P. R., MacDonald C. Disproportionate intentional spatial-memory impairments in amnesia. Neuropsychologia. 1991;29(8):771–784. doi: 10.1016/0028-3932(91)90071-f. [DOI] [PubMed] [Google Scholar]
  36. McCarthy R. A., Evans J. J., Hodges J. R. Topographic amnesia: spatial memory disorder, perceptual dysfunction, or category specific semantic memory impairment? J Neurol Neurosurg Psychiatry. 1996 Mar;60(3):318–325. doi: 10.1136/jnnp.60.3.318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Mellet E., Briscogne S., Tzourio-Mazoyer N., Ghaëm O., Petit L., Zago L., Etard O., Berthoz A., Mazoyer B., Denis M. Neural correlates of topographic mental exploration: the impact of route versus survey perspective learning. Neuroimage. 2000 Nov;12(5):588–600. doi: 10.1006/nimg.2000.0648. [DOI] [PubMed] [Google Scholar]
  38. Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg. 1972;19:421–446. doi: 10.1093/neurosurgery/19.cn_suppl_1.421. [DOI] [PubMed] [Google Scholar]
  39. Morris R. G., Garrud P., Rawlins J. N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982 Jun 24;297(5868):681–683. doi: 10.1038/297681a0. [DOI] [PubMed] [Google Scholar]
  40. Nelson H. E. A modified card sorting test sensitive to frontal lobe defects. Cortex. 1976 Dec;12(4):313–324. doi: 10.1016/s0010-9452(76)80035-4. [DOI] [PubMed] [Google Scholar]
  41. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971 Nov;34(1):171–175. doi: 10.1016/0006-8993(71)90358-1. [DOI] [PubMed] [Google Scholar]
  42. Orsini A., Grossi D., Capitani E., Laiacona M., Papagno C., Vallar G. Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. Ital J Neurol Sci. 1987 Dec;8(6):539–548. doi: 10.1007/BF02333660. [DOI] [PubMed] [Google Scholar]
  43. PALLIS C. A. Impaired identification of faces and places with agnosia for colours; report of a case due to cerebral embolism. J Neurol Neurosurg Psychiatry. 1955 Aug;18(3):218–224. doi: 10.1136/jnnp.18.3.218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pai M. C. Topographic disorientation: two cases. J Formos Med Assoc. 1997 Aug;96(8):660–663. [PubMed] [Google Scholar]
  45. Rolls E. T., Miyashita Y., Cahusac P. M., Kesner R. P., Niki H., Feigenbaum J. D., Bach L. Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown. J Neurosci. 1989 Jun;9(6):1835–1845. doi: 10.1523/JNEUROSCI.09-06-01835.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Ross E. D. Sensory-specific and fractional disorders of recent memory in man. I. Isolated loss of visual recent memory. Arch Neurol. 1980 Apr;37(4):193–200. doi: 10.1001/archneur.1980.00500530031001. [DOI] [PubMed] [Google Scholar]
  47. Snodgrass J. G., Vanderwart M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol Hum Learn. 1980 Mar;6(2):174–215. doi: 10.1037//0278-7393.6.2.174. [DOI] [PubMed] [Google Scholar]
  48. Squire L. R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992 Apr;99(2):195–231. doi: 10.1037/0033-295x.99.2.195. [DOI] [PubMed] [Google Scholar]
  49. Takahashi N., Kawamura M., Shiota J., Kasahata N., Hirayama K. Pure topographic disorientation due to right retrosplenial lesion. Neurology. 1997 Aug;49(2):464–469. doi: 10.1212/wnl.49.2.464. [DOI] [PubMed] [Google Scholar]
  50. Teng E., Squire L. R. Memory for places learned long ago is intact after hippocampal damage. Nature. 1999 Aug 12;400(6745):675–677. doi: 10.1038/23276. [DOI] [PubMed] [Google Scholar]
  51. Whiteley A. M., Warrington E. K. Selective impairment of topographical memory: a single case study. J Neurol Neurosurg Psychiatry. 1978 Jun;41(6):575–578. doi: 10.1136/jnnp.41.6.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Zola-Morgan S. M., Squire L. R. The primate hippocampal formation: evidence for a time-limited role in memory storage. Science. 1990 Oct 12;250(4978):288–290. doi: 10.1126/science.2218534. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Neurology, Neurosurgery, and Psychiatry are provided here courtesy of BMJ Publishing Group

RESOURCES