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Topographical disorientation in aging. Familiarity with the environment does matter

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Abstract

Topographical disorientation (TD) refers to navigational impairment as an effect of aging or brain damage. Decreases in navigational performance with aging are more due to deficits in the ability to mentally represent space in an object-centered (allocentric) than in a self-centered (egocentric) format. Familiarity/remoteness of spatial memory traces can represent a protective factor for TD in aging. Conversely, using newly learned information for assessment may lead to overestimating TD severity as it combines two contributing factors: heading (allocentric) disorientation and anterograde agnosia. A supplementary evaluation of TD with aging according to ecological spatial tasks is recommended. The core tasks should focus on landmark positioning, both on a blind map (allocentric) and along a route (egocentric) of the hometown so as to disentangle spatial memory for familiar/remote information from decline due to recent encoding of information.

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References

  1. Klencklen G, Després O, Dufour A (2012) What do we know about aging and spatial cognition? Reviews and perspectives. Ageing Res Rev 11(1):123–135. https://doi.org/10.1016/j.arr.2011.10.001

    Article  PubMed  Google Scholar 

  2. Postma A, van der Ham I J M (2016) Neuropsychology of space: spatial functions of the human brain. Academic Press

  3. Moffat SD (2009) Aging and spatial navigation: what do we know and where do we go? Neuropsychol Rev 19(4):478–489. https://doi.org/10.1007/s11065-009-9120-3

    Article  PubMed  Google Scholar 

  4. Aguirre GK, D'Esposito M (1999) Topographical disorientation: a synthesis and taxonomy. Brain 122(9):1613–1628. https://doi.org/10.1093/brain/122.9.1613

    Article  PubMed  Google Scholar 

  5. Giovagnoli AR, Manfredi V, Parente A, Schifano L, Oliveri S, Avanzini G (2017) Cognitive training in Alzheimer’s disease: a controlled randomized study. Neurol Sci 38(8):1485–1493. https://doi.org/10.1007/s10072-017-3003-9

    Article  PubMed  CAS  Google Scholar 

  6. Ferrari C, Nacmias B, Sorbi S (2018) The diagnosis of dementias: a practical tool not to miss rare causes. Neurol Sci 39(4):615–627. https://doi.org/10.1007/s10072-017-3206-0

    Article  PubMed  Google Scholar 

  7. Stanzani Maserati M, D’Onofrio R, Matacena C, Sambati L, Oppi F, Poda R, Capellari S (2018) Human figure drawing distinguishes Alzheimer’s patients: a cognitive screening test study. Neurol Sci 39:1–5. https://doi.org/10.1007/s10072-018-3288-3

    Article  Google Scholar 

  8. Grossi D, Fasanaro AM, Cecere R, Salzano S, Trojano L (2007) Progressive topographical disorientation: a case of focal Alzheimer’s disease. Neurol Sci 28(2):107–110. https://doi.org/10.1007/s10072-007-0797-x

    Article  PubMed  CAS  Google Scholar 

  9. Burgess N, Trinkler I, King J, Kennedy A, Cipolotti L (2006) Impaired allocentric spatial memory underlying topographical disorientation. Rev Neurosci 17(1–2):239–251. https://doi.org/10.1515/REVNEURO.2006.17.1-2.239.

    Article  PubMed  Google Scholar 

  10. Pai MC, Hsiao S (2002) Incipient symptoms of alzheimer’s disease and effect of education on the onset age: a study of 155 taiwanese patients. Acta Neurol Taiwanica 11(2):66–69

    Google Scholar 

  11. Pai MC, Jacobs WJ (2004) Topographical disorientation in community-residing patients with Alzheimer’s disease. Int J Geriatr Psychiatry 19:250–255. https://doi.org/10.1002/gps.1081

    Article  PubMed  Google Scholar 

  12. Iachini T, Iavarone A, Senese VP, Ruotolo F, Ruggiero G (2009) Visuospatial memory in healthy elderly, AD and MCI: a review. Curr Aging Sci 2(1):43–59. https://doi.org/10.2174/1874609810902010043

    Article  PubMed  Google Scholar 

  13. Wolbers T, Dudchenko PA, Wood ER (2014) Spatial memory—a unique window into healthy and pathological aging. Front Aging Neurosci 6(MAR). https://doi.org/10.3389/fnagi.2014.00035.

  14. Mandal PK, Joshi J, Saharan S (2012) Visuospatial perception: an emerging biomarker for alzheimer’s disease. J Alzheimers Dis 31(SUPPL. 3):S117–S135. https://doi.org/10.3233/JAD-2012-120901.

    Article  PubMed  Google Scholar 

  15. Lester AW, Moffat SD, Wiener JM, Barnes CA, Wolbers T (2017) The aging navigational system. Neuron 95(5):1019–1035. https://doi.org/10.1016/j.neuron.2017.06.037

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Guariglia CC, Nitrini R (2009) Topographical disorientation in alzheimer’s disease. Arq Neuropsiquiatr 67(4):967–972. https://doi.org/10.1590/S0004-282X2009000600001

    Article  PubMed  Google Scholar 

  17. Tu S, Wong S, Hodges JR, Irish M, Piguet O, Hornberger M (2015) Lost in spatial translation—a novel tool to objectively assess spatial disorientation in Alzheimer’s disease and frontotemporal dementia. Cortex 67:83–94. https://doi.org/10.1016/j.cortex.2015.03.016

    Article  PubMed  Google Scholar 

  18. Lithfous S, Dufour A, Després O (2013) Spatial navigation in normal aging and the prodromal stage of alzheimer’s disease: insights from imaging and behavioral studies. Ageing Res Rev 12(1):201–213. https://doi.org/10.1016/j.arr.2012.04.007

    Article  PubMed  Google Scholar 

  19. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Phelps CH (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. Alzheimers Dement 7(3):270–279. https://doi.org/10.1016/j.jalz.2011.03.008

    Article  PubMed  PubMed Central  Google Scholar 

  20. Park S, Lee J, Lee K, Kim J (2018) Comparison of odor identification among amnestic and non-amnestic mild cognitive impairment, subjective cognitive decline, and early Alzheimer’s dementia. Neurol Sci 39(3):557–564. https://doi.org/10.1007/s10072-018-3261-1

    Article  PubMed  Google Scholar 

  21. Lim TS, Iaria G, Moo SY (2010) Topographical disorientation in mild cognitive impairment: a voxel-based morphometry study. J Clin Neurol 6(4):204–211. https://doi.org/10.3988/jcn.2010.6.4.204

    Article  PubMed  PubMed Central  Google Scholar 

  22. DeIpolyi AR, Rankin KP, Mucke L, Miller BL, Gorno-Tempini ML (2007) Spatial cognition and the human navigation network in AD and MCI. Neurology 69(10):986–997. https://doi.org/10.1212/01.wnl.0000271376.19515.c6

    Article  PubMed  CAS  Google Scholar 

  23. Hort J, Laczó J, Vyhnálek M, Bojar M, Bureš J, Vlček K (2007) Spatial navigation deficit in amnestic mild cognitive impairment. Proc Natl Acad Sci U S A 104(10):4042–4047. https://doi.org/10.1073/pnas.0611314104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Iachini T, Ruggiero G, Ruotolo F (2009) The effect of age on egocentric and allocentric spatial frames of reference. Cogn Process 10(2):222–224. https://doi.org/10.1007/s10339-009-0276-9

    Article  Google Scholar 

  25. Weniger G, Ruhleder M, Wolf S, Lange C, Irle E (2009) Egocentric memory impaired and allocentric memory intact as assessed by virtual reality in subjects with unilateral parietal cortex lesions. Neuropsychologia 47(1):59–69. https://doi.org/10.1016/j.neuropsychologia.2008.08.018

    Article  PubMed  Google Scholar 

  26. Wolf H, Jelic V, Gertz HJ, Nordberg A, Julin P, Wahlund LO (2003) A critical discussion of the role of neuroimaging in mild cognitive impairment. Acta Neurol Scand 107(Suppl. 179):52–76. https://doi.org/10.1034/j.1600-0404.107.s179.10.x.

    Article  Google Scholar 

  27. Laczo J, Vlcek K, Vyhnalek M, Vajnerova O, Ort M, Holmerova I, Tolar M, Andel R, Bojar M, Hort J (2009) Spatial navigation testing discriminates two types of amnestic mild cognitive impairment. Behav Brain Res 202(2):252–259. https://doi.org/10.1016/j.bbr.2009.03.041

    Article  PubMed  Google Scholar 

  28. Weniger G, Ruhleder M, Lange C, Wolf S, Irle E (2011) Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment. Neuropsychologia 49(3):518–527. https://doi.org/10.1016/j.neuropsychologia.2010.12.031

    Article  PubMed  Google Scholar 

  29. Caffò AO, De Caro MF, Picucci L, Notarnicola A, Settanni A, Livrea P, Lancioni GE, Bosco A (2012) Reorientation deficits are associated with amnestic mild cognitive impairment. Am J Alzheimers Dis Other Demen 27(5):321–330. https://doi.org/10.1177/1533317512452035

    Article  PubMed  Google Scholar 

  30. Caffò A O, Lopez A, Spano G, Serino S, Cipresso P, Stasolla F, … Bosco A (2017) Spatial reorientation decline in aging: the combination of geometry and landmarks. Aging Ment Health 1-12. doi:https://doi.org/10.1080/13607863.2017.1354973

  31. Benke T, Karner E, Petermichl S, Prantner V, Kemmler G (2014) Neuropsychological deficits associated with route learning in alzheimer disease, MCI, and normal aging. Alzheimer Dis Assoc Disord 28(2):162–167. https://doi.org/10.1097/WAD.0000000000000009

    Article  PubMed  CAS  Google Scholar 

  32. Rusconi ML, Suardi A, Zanetti M, Rozzini L (2015) Spatial navigation in elderly healthy subjects, amnestic and non amnestic MCI patients. J Neurol Sci 359(1–2):430–437. https://doi.org/10.1016/j.jns.2015.10.010

    Article  PubMed  Google Scholar 

  33. Chipi E, Frattini G, Eusebi P, Mollica A, D’Andrea K, Russo M, Parnetti L (2018) The Italian version of cognitive function instrument (CFI): reliability and validity in a cohort of healthy elderly. Neurol Sci 39(1):111–118. https://doi.org/10.1007/s10072-017-3150-z

    Article  PubMed  Google Scholar 

  34. Serino S, Morganti F, Di Stefano F, Riva G (2015) Detecting early egocentric and allocentric impairments deficits in Alzheimer’s disease: an experimental study with virtual reality. Front Aging Neurosci 7. doi:https://doi.org/10.3389/fnagi.2015.00088.

  35. Boccia M, Silveri MC, Sabatini U, Guariglia C, Nemmi F (2016) Neural underpinnings of the decline of topographical memory in mild cognitive impairment. Am J Alzheimers Dis Other Demen 31(8):618–630. https://doi.org/10.1177/1533317516654757

    Article  PubMed  Google Scholar 

  36. Ekstrom AD, Arnold AE, Iaria G (2014) A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective. Front Hum Neurosci 8:803. https://doi.org/10.3389/fnhum.2014.00803

    Article  PubMed  PubMed Central  Google Scholar 

  37. Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9(3):nrn2335. https://doi.org/10.1038/nrn2335

    Article  CAS  Google Scholar 

  38. Evans GW, Pezdek K (1980) Cognitive mapping: knowledge of real-world distance and location information. J Exp Psychol Hum Learn 6(1):13–24. https://doi.org/10.1037/0278-7393.6.1.13

    Article  PubMed  CAS  Google Scholar 

  39. Thorndyke PW, Hayes-Roth B (1982) Differences in spatial knowledge acquired from maps and navigation. Cogn Psychol 14(4):560–589. https://doi.org/10.1016/0010-0285(82)90019-6

    Article  PubMed  CAS  Google Scholar 

  40. Kirasic KC (1991) Spatial cognition and behavior in young and elderly adults: implications for learning new environments. Psychol Aging 6(1):10–18. https://doi.org/10.1037/0882-7974.6.1.10

    Article  PubMed  CAS  Google Scholar 

  41. Iachini T, Borghi AM, Senese VP (2008) Categorization and sensorimotor interaction with objects. Brain Cogn 67(1):31–43. https://doi.org/10.1016/j.bandc.2007.11.002

    Article  PubMed  Google Scholar 

  42. Rosenbaum R S, Winocur G, Binns M A, Moscovitch M (2012) Remote spatial memory in aging: all is not lost. Front Aging Neurosci 4. doi: https://doi.org/10.3389/fnagi.2012.00025

  43. Meneghetti C, Borella E, Fiore F, De Beni R (2013) The ability to point to well-known places in young and older adults. Aging Clin Exp Res 25(2):203–209. https://doi.org/10.1007/s40520-013-0027-8

    Article  PubMed  Google Scholar 

  44. Campbell JI, Hepner IJ, Miller LA (2014) The influence of age and sex on memory for a familiar environment. J Environ Psychol 40:1–8. https://doi.org/10.1016/j.jenvp.2014.04.007

    Article  Google Scholar 

  45. Muffato V, Della Giustina M, Meneghetti C, De Beni R (2015) Age-related differences in pointing accuracy in familiar and unfamiliar environments. Cogn Process 16(1):313–317. https://doi.org/10.1007/s10339-015-0720-y

    Article  PubMed  Google Scholar 

  46. Merriman NA, Ondřej J, Roudaia E, O’Sullivan C, Newell FN (2016) Familiar environments enhance object and spatial memory in both younger and older adults. Exp Brain Res 234(6):1555–1574. https://doi.org/10.1007/s00221-016-4557-0

    Article  PubMed  Google Scholar 

  47. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford: Clarendon Press

  48. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641. https://doi.org/10.1016/S0896-6273(02)00830-9

    Article  PubMed  CAS  Google Scholar 

  49. Maguire EA, Woollett K, Spiers HJ (2006) London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 16(12):1091–1101. https://doi.org/10.1002/hipo.20233

    Article  PubMed  Google Scholar 

  50. Rosenbaum RS, Priselac S, Köhler S, Black SE, Gao F, Nadel L, Moscovitch M (2000) Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions. Nat Neurosci 3(10):1044–1048. https://doi.org/10.1038/79867

    Article  PubMed  CAS  Google Scholar 

  51. Maguire EA, Vargha-Khadem F, Mishkin M (2001) The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124:1156–1170. https://doi.org/10.1093/brain/124.6.1156

    Article  PubMed  CAS  Google Scholar 

  52. Burgess N, Becker S, King JA, O'Keefe J (2001) Memory for events and their spatial context: models and experiments. Philos Trans R Soc B Biol Sci 356(1413):1493–1503. https://doi.org/10.1098/rstb.2001.0948

    Article  CAS  Google Scholar 

  53. Rosenbaum RS, Gao F, Richards B, Black SE, Moscovitch M (2005) ‘Where to?’ Remote memory for spatial relations and landmark identity in former taxi drivers with Alzheimer’s disease and encephalitis. J Cogn Neurosci 17(3):446–462. https://doi.org/10.1162/0898929053279496

    Article  PubMed  Google Scholar 

  54. Moscovitch M, Rosenbaum RS, Addis DR, Westmacott R, Grady C, McAndrews MP, Levine B, Black S, Winocur G, Nadel L (2005) Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 207(1):35–66. https://doi.org/10.1111/j.1469-7580.2005.00421.x

    Article  PubMed  PubMed Central  Google Scholar 

  55. Winocur G, Moscovitch M, Sekeres M (2007) Memory consolidation or transformation: context manipulation and hippocampal representations of memory. Nat Neurosci 10(5):555–557. https://doi.org/10.1038/nn1880

    Article  PubMed  CAS  Google Scholar 

  56. Hirshhorn M, Newman L, Moscovitch M (2011) Detailed descriptions of routes traveled, but not map-like knowledge, correlates with tests of hippocampal function in older adults. Hippocampus 21(11):1147–1151. https://doi.org/10.3389/fnagi.2012.00025

    Article  PubMed  Google Scholar 

  57. Boccia M, Nemmi F, Guariglia C (2014) Neuropsychology of environmental navigation in humans: review and meta-analysis of FMRI studies in healthy participants. Neuropsychol Rev 24(2):236–251. https://doi.org/10.1007/s11065-014-9247-8

    Article  PubMed  PubMed Central  Google Scholar 

  58. Serino S, Cipresso P, Morganti F, Riva G (2014) The role of egocentric and allocentric abilities in Alzheimer’s disease: a systematic review. Ageing Res Rev 16(1):32–44. https://doi.org/10.1016/j.arr.2014.04.004.

    Article  PubMed  Google Scholar 

  59. Ruggiero G, D’Errico O, Iachini T (2016) Development of egocentric and allocentric spatial representations from childhood to elderly age. Psychol Res 80(2):259–272. https://doi.org/10.1007/s00426-015-0658-9

    Article  PubMed  Google Scholar 

  60. Bosco A, Picucci L, Caffò AO, Lancioni GE, Gyselinck V (2008) Assessing human reorientation ability inside virtual reality environments: the effects of retention interval and landmark characteristics. Cogn Process 9(4):299–309. https://doi.org/10.1007/s10339-008-0210-6

    Article  PubMed  Google Scholar 

  61. Barrash J (1994) Age-related decline in route learning ability. Dev Neuropsychol 10(3):189–201. https://doi.org/10.1080/87565649409540578

    Article  Google Scholar 

  62. Kirasic KC, Mathes EA (1990) Effects of different means for conveying environmental information on elderly adults’ spatial cognition and behavior. Environ Behav 22(5):591–607. https://doi.org/10.1177/0013916590225002

    Article  Google Scholar 

  63. Boccia M, Vecchione F, Piccardi L, Guariglia C (2017) Effect of cognitive style on learning and retrieval of navigational environments. Front Pharmacol 8:496. https://doi.org/10.3389/fphar.2017.00496

    Article  PubMed  PubMed Central  Google Scholar 

  64. Tlauka M (2006) Orientation dependent mental representations following real-world navigation. Scand J Psychol 47(3):171–176. https://doi.org/10.1111/j.1467-9450.2006.00504.x

    Article  PubMed  Google Scholar 

  65. Waller D (2005) The WALKABOUT: using virtual environments to assess large-scale spatial abilities. Comput Hum Behav 21(2):243–253. https://doi.org/10.1016/j.chb.2004.02.022

    Article  Google Scholar 

  66. Picucci L, Caffo AO, Bosco A (2009) Age and sex differences in a virtual version of the reorientation task. Cogn Process 10(2):272–275. https://doi.org/10.1007/s10339-009-0321-8

    Article  Google Scholar 

  67. Bosco A, Longoni AM, Vecchi T (2004) Gender effects in spatial orientation: cognitive profiles and mental strategies. Appl Cogn Psychol 18(5):519–532. https://doi.org/10.1002/acp.1000

    Article  PubMed  PubMed Central  Google Scholar 

  68. Coluccia E, Bosco A, Brandimonte MA (2007) The role of visuo-spatial working memory in map learning: new findings from a map drawing paradigm. Psychol Res 71(3):359–372. https://doi.org/10.1007/s00426-006-0090-2

    Article  PubMed  Google Scholar 

  69. Lynch K (1960) The Image of the City. The MIT Press

  70. Broadbent G, Bunt R, Jencks C (1980) Signs, symbols, and architecture. John Wiley & Sons

  71. Lopez A, Caffò A O, Spano G, Bosco A (2019) The effect of aging on memory for recent and remote egocentric and allocentric information. Exp Aging Res in press

  72. Caduff D, Timpf S (2008) On the assessment of landmark salience for human navigation. Cogn Process 9(4):249–267. https://doi.org/10.1007/s10339-007-0199-2

    Article  PubMed  Google Scholar 

  73. Götze J, Boye J (2016) Learning landmark salience models from users’ route instructions. J Locat Based Serv 10(1):47–63. https://doi.org/10.1080/17489725.2016.1172739

    Article  Google Scholar 

  74. Röser F, Krumnack A, Hamburger K, Knauff M (2012) A four factor model of landmark salience—a new approach. In Proceedings of the 11th International Conference on Cognitive Modeling (ICCM) 82–87

  75. Nemmi F, Piras F, Péran P, Incoccia C, Sabatini U, Guariglia C (2013) Landmark sequencing and route knowledge: an fMRI study. Cortex 49(2):507–519. https://doi.org/10.1016/j.cortex.2011.11.016

    Article  PubMed  Google Scholar 

  76. Caffò AO, Hoogeveen F, Groenendaal M, Perilli AV, Picucci L, Lancioni GE, Bosco A (2014) Intervention strategies for spatial orientation disorders in dementia: a selective review. Dev Neurorehabil 17(3):200–209. https://doi.org/10.3109/17518423.2012.749951

    Article  PubMed  Google Scholar 

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Funding

The second author (AOC) was supported by the project “Epidemiology of Topographical Disorientation and Mild Cognitive Impairment in a South Italian elderly population” - Action Co-founded by Cohesion and Development Fund 2007–2013 - APQ Research Puglia Region “Regional programme supporting smart specialization and social and environmental sustainability - FutureInResearch” (Grant Code CEY4SQ4). All the authors contributed to the conception, drafting and revising the work.

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  1. Department of Educational Sciences, Psychology, Communication, University of Studies of Bari, Via Crisanzio 42, 70122, Bari, Italy

    Antonella Lopez, Alessandro O. Caffò & Andrea Bosco

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Correspondence to Andrea Bosco.

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Lopez, A., Caffò, A.O. & Bosco, A. Topographical disorientation in aging. Familiarity with the environment does matter. Neurol Sci 39, 1519–1528 (2018). https://doi.org/10.1007/s10072-018-3464-5

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