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Open Access 08-05-2023 | Amyotrophic Lateral Sclerosis | Original Communication

Memory-guided navigation in amyotrophic lateral sclerosis

Authors: Patrizia M. Maier, Deetje Iggena, Thomas Meyer, Carsten Finke, Christoph J. Ploner

Published in: Journal of Neurology | Issue 8/2023

Abstract

Background

Previous studies have yielded inconsistent results about hippocampal involvement in non-demented patients with amyotrophic lateral sclerosis (ALS). We hypothesized that testing of memory-guided spatial navigation i.e., a highly hippocampus-dependent behaviour, might reveal behavioural correlates of hippocampal dysfunction in non-demented ALS patients.

Methods

We conducted a prospective study of spatial cognition in 43 non-demented ALS outpatients (11f, 32 m, mean age 60.0 years, mean disease duration 27.0 months, mean ALSFRS-R score 40.0) and 43 healthy controls (14f, 29 m, mean age 57.0 years). Participants were tested with a virtual memory-guided navigation task derived from animal research (“starmaze”) that has previously been used in studies of hippocampal function. Participants were further tested with neuropsychological tests of visuospatial memory (SPART, 10/36 Spatial Recall Test), fluency (5PT, five-point test) and orientation (PTSOT, Perspective Taking/Spatial Orientation Test).

Results

Patients successfully learned and navigated the starmaze from memory, both in conditions that forced memory of landmarks (success: patients 50.7%, controls 47.7%, p = 0.786) and memory of path sequences (success: patients 96.5%, controls 94.0%, p = 0.937). Measures of navigational efficacy (latency, path error and navigational uncertainty) did not differ between groups (p ≥ 0.546). Likewise, SPART, 5PT and PTSOT scores did not differ between groups (p ≥ 0.238).

Conclusions

This study found no behavioural correlate for hippocampal dysfunction in non-demented ALS patients. These findings support the view that the individual cognitive phenotype of ALS may relate to distinct disease subtypes rather than being a variable expression of the same underlying condition.

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van Es MA, Hardiman O, Chiò A et al (2017) Amyotrophic lateral sclerosis. Lancet 390:2084–2098. https://doi.org/10.1016/S0140-6736(17)31287-4CrossRefPubMed

Phukan J, Elamin M, Bede P et al (2012) The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J Neurol Neurosurg Psychiatry 83:102–108. https://doi.org/10.1136/jnnp-2011-300188CrossRefPubMed

Montuschi A, Iazzolino B, Calvo A et al (2015) Cognitive correlates in amyotrophic lateral sclerosis: a population-based study in Italy. J Neurol Neurosurg Psychiatry 86:168–173. https://doi.org/10.1136/jnnp-2013-307223CrossRefPubMed

Chiò A, Moglia C, Canosa A et al (2019) Cognitive impairment across ALS clinical stages in a population-based cohort. Neurology 93:E984–E994. https://doi.org/10.1212/WNL.0000000000008063CrossRefPubMedPubMedCentral

Ahmed RM, Bocchetta M, Todd EG et al (2021) Tackling clinical heterogeneity across the amyotrophic lateral sclerosis–frontotemporal dementia spectrum using a transdiagnostic approach. Brain Commun 3:1–14. https://doi.org/10.1093/braincomms/fcab257CrossRef

Burrell JR, Halliday GM, Kril JJ et al (2016) The frontotemporal dementia-motor neuron disease continuum. Lancet 388:919–931. https://doi.org/10.1016/S0140-6736(16)00737-6CrossRefPubMed

Crockford C, Newton J, Lonergan K et al (2018) ALS-specific cognitive and behavior changes associated with advancing disease stage in ALS. Neurology 91:E1370–E1380. https://doi.org/10.1212/WNL.0000000000006317CrossRefPubMedPubMedCentral

Abdulla S, Machts J, Kaufmann J et al (2014) Hippocampal degeneration in patients with amyotrophic lateral sclerosis. Neurobiol Aging 35:2639–2645. https://doi.org/10.1016/j.neurobiolaging.2014.05.035CrossRefPubMed

Barulli MR, Piccininni M, Di Dio C et al (2019) Episodic memory and learning rates in amyotrophic lateral sclerosis without dementia. Cortex 117:257–265. https://doi.org/10.1016/j.cortex.2019.03.003CrossRefPubMed

10.

Machts J, Keute M, Kaufmann J et al (2021) Longitudinal clinical and neuroanatomical correlates of memory impairment in motor neuron disease. NeuroImage Clin 29:102545. https://doi.org/10.1016/j.nicl.2020.102545CrossRefPubMed

11.

Consonni M, Rossi S, Cerami C et al (2017) Executive dysfunction affects word list recall performance: evidence from amyotrophic lateral sclerosis and other neurodegenerative diseases. J Neuropsychol 11:74–90. https://doi.org/10.1111/JNP.12072CrossRefPubMed

12.

Raaphorst J, van Tol MJ, de Visser M et al (2015) Prose memory impairment in amyotrophic lateral sclerosis patients is related to hippocampus volume. Eur J Neurol 22:547–554. https://doi.org/10.1111/ene.12615CrossRefPubMed

13.

Christidi F, Karavasilis E, Velonakis G et al (2018) The clinical and radiological spectrum of hippocampal pathology in amyotrophic lateral sclerosis. Front Neurol 9:1–11. https://doi.org/10.3389/fneur.2018.00523CrossRef

14.

Consonni M, Dalla Bella E, Bersano E et al (2021) Cognitive reserve is associated with altered clinical expression in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Front Degener 22:237–247. https://doi.org/10.1080/21678421.2020.1849306CrossRef

15.

Nyberg N, Duvelle É, Barry C, Spiers HJ (2022) Spatial goal coding in the hippocampal formation. Neuron 110:394–422. https://doi.org/10.1016/J.NEURON.2021.12.012CrossRefPubMed

16.

Chersi F, Burgess N (2015) The cognitive architecture of spatial navigation: hippocampal and striatal contributions. Neuron 88:64–77. https://doi.org/10.1016/j.neuron.2015.09.021CrossRefPubMed

17.

Ekstrom AD, Huffman DJ, Starrett M (2017) Interacting networks of brain regions underlie human spatial navigation: a review and novel synthesis of the literature. J Neurophysiol 118:3328–3344. https://doi.org/10.1152/jn.00531.2017CrossRefPubMedPubMedCentral

18.

Coughlan G, Laczó J, Hort J et al (2018) Spatial navigation deficits—overlooked cognitive marker for preclinical Alzheimer disease? Nat Rev Neurol 14:496–506. https://doi.org/10.1038/S41582-018-0031-XCrossRefPubMed

19.

Iglói K, Zaoui M, Berthoz A, Rondi-Reig L (2009) Sequential egocentric strategy is acquired as early as allocentric strategy: parallel acquisition of these two navigation strategies. Hippocampus 19:1199–1211. https://doi.org/10.1002/hipo.20595CrossRefPubMed

20.

Iglói K, Doeller CF, Berthoz A et al (2010) Lateralized human hippocampal activity predicts navigation based on sequence or place memory. Proc Natl Acad Sci USA 107:14466–14471. https://doi.org/10.1073/pnas.1004243107CrossRefPubMedPubMedCentral

21.

Iggena D, Maier PM, Häußler SM et al (2022) Post-encoding modulation of spatial memory consolidation by propofol. Cortex 156:1–12. https://doi.org/10.1016/j.cortex.2022.08.004CrossRefPubMed

22.

Shefner JM, Al-Chalabi A, Baker MR et al (2020) A proposal for new diagnostic criteria for ALS. Clin Neurophysiol 131:1975–1978. https://doi.org/10.1016/j.clinph.2020.04.005CrossRefPubMed

23.

Cedarbaum JM, Stambler N, Malta E et al (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. J Neurol Sci 169:13–21. https://doi.org/10.1016/S0022-510X(99)00210-5CrossRefPubMed

24.

Strong MJ, Abrahams S, Goldstein LH et al (2017) Amyotrophic lateral sclerosis—frontotemporal spectrum disorder (ALS-FTSD): revised diagnostic criteria. Amyotroph Lateral Scler Front Degener 18:153–174. https://doi.org/10.1080/21678421.2016.1267768CrossRef

25.

Rascovsky K, Hodges JR, Knopman D et al (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134:2456–2477. https://doi.org/10.1093/brain/awr179CrossRefPubMedPubMedCentral

26.

Abrahams S, Newton J, Niven E et al (2014) Screening for cognition and behaviour changes in ALS. Amyotroph Lateral Scler Front Degener 15:9–14. https://doi.org/10.3109/21678421.2013.805784CrossRef

27.

Goebel S, Fischer R, Ferstl R, Mehdorn HM (2009) Normative data and psychometric properties for qualitative and quantitative scoring criteria of the five-point test. Clin Neuropsychol 23:675–690. https://doi.org/10.1080/13854040802389185CrossRefPubMed

28.

Scherer P, Baum K, Bauer H et al (2004) Normalization of the Brief Repeatable Battery of Neuropsychological tests (BRB-N) for German-speaking regions. Application in relapsing-remitting and secondary progressive multiple sclerosis patients. Nervenarzt 75:984–990. https://doi.org/10.1007/S00115-004-1729-0CrossRefPubMed

29.

Hegarty M, Waller D (2004) A dissociation between mental rotation and perspective-taking spatial abilities. Intelligence 32:175–191. https://doi.org/10.1016/J.INTELL.2003.12.001CrossRef

30.

Hegarty M, Richardson AE, Montello DR et al (2002) Development of a self-report measure of environmental spatial ability. Intelligence 30:425–447. https://doi.org/10.1016/S0160-2896(02)00116-2CrossRef

31.

Rondi-Reig L, Petit GH, Tobin C et al (2006) Impaired sequential egocentric and allocentric memories in forebrain-specific-NMDA receptor knock-out mice during a new task dissociating strategies of navigation. J Neurosci 26:4071–4081. https://doi.org/10.1523/JNEUROSCI.3408-05.2006CrossRefPubMedPubMedCentral

32.

Brookes J, Warburton M, Alghadier M et al (2019) Studying human behavior with virtual reality: the unity experiment framework. Behav Res Methods 52:455–463. https://doi.org/10.3758/S13428-019-01242-0CrossRefPubMedCentral

33.

Garthe A, Kempermann G (2013) An old test for new neurons: refining the morris water maze to study the functional relevance of adult hippocampal neurogenesis. Front Neurosci 7:1–11. https://doi.org/10.3389/fnins.2013.00063CrossRef

34.

Maei HR, Zaslavsky K, Teixeira CM, Frankland PW (2009) What is the most sensitive measure of water maze probe test performance? Front Integr Neurosci 3:1–9. https://doi.org/10.3389/neuro.07.004.2009CrossRef

35.

Gardony AL, Taylor HA, Brunyé TT (2016) Gardony map drawing analyzer: software for quantitative analysis of sketch maps. Behav Res Methods 48:151–177. https://doi.org/10.3758/S13428-014-0556-XCrossRefPubMed

36.

Machts J, Vielhaber S, Kollewe K et al (2018) Global hippocampal volume reductions and local CA1 shape deformations in Amyotrophic Lateral Sclerosis. Front Neurol 9:1–9. https://doi.org/10.3389/fneur.2018.00565CrossRef

37.

Trojsi F, Di Nardo F, Siciliano M et al (2021) Frontotemporal degeneration in amyotrophic lateral sclerosis (ALS): a longitudinal MRI one-year study. CNS Spectr 26:258–267. https://doi.org/10.1017/S109285292000005XCrossRefPubMed

38.

Bellassen V, Iglói K, Cruz de Souza L et al (2012) Temporal order memory assessed during spatiotemporal navigation as a behavioral cognitive marker for differential Alzheimer’s disease diagnosis. J Neurosci 32:1942–1952. https://doi.org/10.1523/JNEUROSCI.4556-11.2012CrossRefPubMedPubMedCentral

39.

Kasper E, Zydatiss K, Schuster C et al (2016) No change in executive performance in ALS patients: a longitudinal neuropsychological study. Neurodegener Dis 16:184–191. https://doi.org/10.1159/000440957CrossRefPubMed

40.

Beeldman E, Govaarts R, De Visser M et al (2020) Progression of cognitive and behavioural impairment in early amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 91:779–780. https://doi.org/10.1136/JNNP-2020-322992CrossRefPubMed

41.

Elamin M, Bede P, Byrne S et al (2013) Cognitive changes predict functional decline in ALS: a population-based longitudinal study. Neurology 80:1590–1597. https://doi.org/10.1212/WNL.0b013e31828f18acCrossRefPubMed

42.

Gregory JM, McDade K, Bak TH et al (2020) Executive, language and fluency dysfunction are markers of localised TDP-43 cerebral pathology in non-demented ALS. J Neurol Neurosurg Psychiatry 91:149–157. https://doi.org/10.1136/jnnp-2019-320807CrossRefPubMed

43.

Consonni M, Catricalà E, Dalla Bella E et al (2016) Beyond the consensus criteria: multiple cognitive profiles in amyotrophic lateral sclerosis? Cortex 81:162–167. https://doi.org/10.1016/j.cortex.2016.04.014CrossRefPubMed

44.

Dukic S, McMackin R, Costello E et al (2022) Resting-state EEG reveals four subphenotypes of amyotrophic lateral sclerosis. Brain 145:621–631. https://doi.org/10.1093/BRAIN/AWAB322CrossRefPubMed

Title: Memory-guided navigation in amyotrophic lateral sclerosis
Authors: Patrizia M. Maier
Deetje Iggena
Thomas Meyer
Carsten Finke
Christoph J. Ploner
Publication date: 08-05-2023
Publisher: Springer Berlin Heidelberg
Keywords: Amyotrophic Lateral Sclerosis
Frontotemporal Dementia
Frontotemporal Dementia
Published in: Journal of Neurology / Issue 8/2023
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-023-11753-8

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Springer Medicine

Memory-guided navigation in amyotrophic lateral sclerosis

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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