Skip to main content
SpringerLink
Log in

Relationship between episodic memory and volume of the brain regions of two functional cortical memory systems in multiple sclerosis

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Background/objective

Two functional networks are proposed as neuronal support for the complex processes of memory: the anterior temporal and the medial posterior systems. We examined the atrophy of hippocampus (HC) and of those areas constituting the two functional memory systems in multiple sclerosis (MS) patients with low disability.

Methods

Episodic memory (EM) was assessed in 88 relapsing MS patients and in 40 healthy controls using Wechsler Memory Scale III (Spanish adaptation). FreeSurfer software was used to calculate normalized volume of total cortex, grey matter, white matter, subcortical grey matter (thalamus and striatum), HC and both the anterior temporal (entorhinal, ventral temporopolar, lateral orbitofrontal, amygdala) and posterior medial systems (thalamus, parahippocampal, posterior cingulate, precuneus, lateral parietal and medial prefrontal). Linear regression analysis was used to identify predictors of memory performance.

Results

Total grey matter and cortex volumes correlated with all subtypes of EM, and the precuneus volume correlated with overall, immediate and delayed memories. Univariant regression analysis identified an association between the volumes of the posterior medial memory network regions and EM scores. The volume of the left precuneus area was the unique and independent predictor for all EM subtypes except for visual memory, for which left HC volume was also an independent predictor.

Conclusion

Left precuneus volume was the best predictor of memory in relapsing MS patients with low disability and mild deficits in EM.

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

Similar content being viewed by others

References

  1. Amato MP, Zipoli V, Portaccio E (2008) Cognitive changes in multiple sclerosis. Expert Rev Neurother 8:1585–1596. https://doi.org/10.1586/14737175.8.10.1585

    Article  PubMed  Google Scholar 

  2. Saenz A, Bakchine S, Jonin PY et al (2015) Multiple sclerosis and verbal episodic memory: critical review of cognitive processes and their assessment. Rev Neurol (Paris) 171:624–645

    Article  CAS  Google Scholar 

  3. Brissart H, Morele E, Baumann C et al (2012) Verbal episodic memory in 426 multiple sclerosis patients: impairment in encoding, retrieval or both? Neurol Sci 33:1117–1123. https://doi.org/10.1007/s10072-011-0915

    Article  CAS  PubMed  Google Scholar 

  4. Travis SG, Huang Y, Fujiwara E et al (2014) High field structural MRI reveals specific episodic memory correlates in the subfields of the hippocampus. Neuropsychologia 53:233–245. https://doi.org/10.1016/j.neuropsychologia.2013.11.016

    Article  CAS  PubMed  Google Scholar 

  5. Griffith HR, Pyzalski RW, Seidenberg M et al (2004) Memory relationships between MRI volumes and resting PET metabolism of medial temporal lobe structures. Epilepsy Behav 5:669–676

    Article  Google Scholar 

  6. Geurts JJ, Bö L, Roosendaal SD et al (2007) Extensive hippocampal demyelination in multiple sclerosis. J Neuropathol Exp Neurol 66:819–827

    Article  Google Scholar 

  7. Papadopoulos D, Dukes S, Patel R et al (2009) Substantial archaeocortical atrophy and neuronal loss in multiple sclerosis. Brain Pathol 19:238–253

    Article  Google Scholar 

  8. Geurts JJ, Pouwels PJ, Uitdehaag BM et al (2005) Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion recovery MR imaging. Radiology 263:254–260

    Article  Google Scholar 

  9. Sicotte NL, Kern KC, Giesser BS et al (2008) Regional hippocampal atrophy in multiple sclerosis. Brain 131:1134–1141

    Article  CAS  Google Scholar 

  10. Benedict RH, Ramasamy D, Munschauer F et al (2009) Memory impairment in multiple sclerosis: correlation with deep grey matter and mesial temporal atrophy. J Neurol Neurosurg Psychiatry 80:201–206

    Article  CAS  Google Scholar 

  11. Longoni G, Rocca MA, Pagani E et al (2015) Deficits in memory and visuospatial learning correlate with regional hippocampal atrophy in MS. Brain Struct Funct 220:435–444

    Article  Google Scholar 

  12. González Torre JA, Cruz-Gómez ÁJ, Belenguer A et al (2017) Hippocampal dysfunction is associated with memory impairment in multiple sclerosis: a volumetric and functional connectivity study. Mult Scler 23:1854–1863. https://doi.org/10.1177/1352458516688349

    Article  PubMed  Google Scholar 

  13. Ranganath C, Ritchey M (2012) Two cortical systems for memory-guided behavior. Nat Rev Neurosci 13:713–726. https://doi.org/10.1038/nrn3338

    Article  CAS  PubMed  Google Scholar 

  14. Ritchey M, Libby LA, Ranganath C (2015) Cortico-hippocampal systems involved in memory and cognition: the PMAT framework. Prog Brain Res 219:45–64. https://doi.org/10.1016/bs.pbr.2015.04.001

    Article  PubMed  Google Scholar 

  15. Sumowski JF, Leavitt VM, Rocca MA et al (2017) Mesial temporal lobe and subcortical grey matter volumes differentially predict memory across stages of multiple sclerosis. Mult Scler. https://doi.org/10.1177/1352458517708873

    Article  PubMed  Google Scholar 

  16. Polman C, Reingold S, Banwell B et al (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292–302

    Article  Google Scholar 

  17. Wechsler D (2004) Wechsler Memory Scale, 3rd edn. TEA Ediciones, Madrid

    Google Scholar 

  18. Schmidt P, Gaser C, Arsic M et al (2012) An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. Neuroimage 59:3774–3783

    Article  Google Scholar 

  19. Pareto D, Sastre-Garriga J, Aymerich FX et al (2016) Lesion filling effect in regional brain volume estimations: a study in multiple sclerosis patients with low lesion load. Neuroradiology 58:467. https://doi.org/10.1007/s00234-016-1654-5

    Article  CAS  PubMed  Google Scholar 

  20. Valverde S, Oliver A, Roura E et al (2015) Quantifying brain tissue volume in multiple sclerosis with automated lesion segmentation and filling. NeuroImage Clin 9:640–647. https://doi.org/10.1016/j.nicl.2015.10.012

    Article  PubMed  PubMed Central  Google Scholar 

  21. Biberacher V, Schmidt P, Keshavan A et al (2016) Intra and interscanner variability of magnetic resonance imaging based volumetry in multiple sclerosis. NeuroImage 142:188–197. https://doi.org/10.1016/j.neuroimage.2016.07.035

    Article  PubMed  Google Scholar 

  22. Magon S, Gaetano L, Chakravarty MM et al (2014) White matter lesion filling improves the accuracy of cortical thickness measurements in multiple sclerosis patients: a longitudinal study. BMC Neurosci 15:106. https://doi.org/10.1186/1471-2202-15-106

    Article  PubMed  PubMed Central  Google Scholar 

  23. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055

    Article  CAS  Google Scholar 

  24. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583. https://doi.org/10.1093/brain/aw1004

    Article  PubMed  Google Scholar 

  25. Utevsky AV, Smith DV, Huettel SA (2014) Precuneus is a functional core of the default-mode network. J Neurosci 34:932–940. https://doi.org/10.1523/JNEUROSCI.4227-13.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Schmidt D, Krause BJ, Mottaghy FM et al (2002) Brain systems engaged in encoding and retrieval of word-pair associates independent of their imagery content or presentation modalities. Neuropsychologia 40:457–470. https://doi.org/10.1016/S0028-3932(01)00102-6

    Article  CAS  PubMed  Google Scholar 

  27. Henson RN, Rugg MD, Shallice T et al (1999) Recollection and familiarity in recognition memory: an event-related functional magnetic resonance imaging study. J Neurosci 19:3962–3972

    Article  CAS  Google Scholar 

  28. Lundstrom BN, Ingvar M, Petersson KM (2005) The role of precuneus and left inferior frontal cortex during source memory episodic retrieval. Neuroimage 27:824–834. https://doi.org/10.1016/j.neuroimage.2005.05.008

    Article  PubMed  Google Scholar 

  29. Peters J, Daum I, Gizewski E et al (2009) Associations evoked during memory encoding recruit the context-network. Hippocampus 19:141–151. https://doi.org/10.1002/hipo.20490

    Article  PubMed  Google Scholar 

  30. Dörfel D, Werner A, Scheafer M et al (2009) Distinct brain networks in recognition memory share a defined region in the precuneus. Eur J Neurosci 30:1947–1959. https://doi.org/10.1111/j.1460-9568.2009.06973.x

    Article  PubMed  Google Scholar 

  31. Eustache F, Piolino P, Giffard B et al (2004) “In the course of time”: a PET study of the cerebral substrates of autobiographical amnesia in Alzheimer’s disease. Brain 127:1549–1560. https://doi.org/10.1093/brain/awh166

    Article  PubMed  Google Scholar 

  32. Bailly M, Destrieux C, Hommet C et al (2015) Precuneus and cingulate cortex atrophy and hypometabolism in patients with Alzheimer’s disease and mild cognitive impairment: MRI and F-18-FDG PET quantitative analysis using freesurfer. Biomed Res Int. https://doi.org/10.1155/2015/583931

    Article  PubMed  PubMed Central  Google Scholar 

  33. Klaassens BL, van Gerven JMA, van der Grond J et al (2017) Diminished posterior precuneus connectivity with the default mode network differentiates normal aging from Alzheimer’s disease. Front Aging Neurosci 9:97. https://doi.org/10.3389/fnagi.2017.00097

    Article  PubMed  PubMed Central  Google Scholar 

  34. Freton M, Lemogne C, Bergouignan L et al (2014) The eye of the self: precuneus volume and visual perspective during autobiographical memory retrieval. Brain Struct Funct 219:959–968. https://doi.org/10.1007/s00429-013-0546-2

    Article  PubMed  Google Scholar 

  35. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to MS patients and HC for their participation.

Funding

This research was supported by Novartis.

Author information

Authors and Affiliations

  1. Multiple Sclerosis Unit, Department of Neurology, Getafe University Hospital, European University of Madrid, Carretera de Toledo km 12,5, 28905, Madrid, Spain

    Yolanda Aladro & Marta Cerezo-García

  2. Faculty of Psychology of the University of Oviedo, Oviedo, Spain

    Laudino López-Alvarez

  3. Department of Radiology, Getafe University Hospital, European University of Madrid, Madrid, Spain

    Jorge Mario Sánchez-Reyes

  4. Radiology and Nuclear Medicine Department, Erasmus MC, Rotterdam, The Netherlands

    Juan Antonio Hernández-Tamames

  5. Laboratorio de Análisis de Imagen Médica y Biometría (LAIMBIO), Rey Juan Carlos University, Móstoles, Madrid, Spain

    Helena Melero

  6. Faculty of Psychology of the Autonoma University of Madrid, Madrid, Spain

    Sandra Rubio-Fernández

  7. Department of Statistic, European University of Madrid, Madrid, Spain

    Israel Thuissard

Authors
  1. Yolanda Aladro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laudino López-Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge Mario Sánchez-Reyes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan Antonio Hernández-Tamames
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Helena Melero
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sandra Rubio-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Israel Thuissard
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marta Cerezo-García
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yolanda Aladro.

Ethics declarations

Conflicts of interest

Authors declare not having conflicts of interest with respect to this work. We report all possible disclosures to be thorough. Y. A. had received speakers’ honoraria from Novartis, Biogen Idec, Teva and Merck Serono; serves as a consultant and scientific advisory board for some Pharmaceutical Industries (Teva, Novartis, Biogen Idec, Sanofi Genzyme and Merck Serono). M. C. received support to investigate from Novartis and Teva.

Ethical standard

All procedures performed in this study involving human participants were carried out respecting the principles established in the 1964 Helsinki Declaration and its later amendments, the requirements by the Spanish legislation on biomedical investigation and protection of personal data.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aladro, Y., López-Alvarez, L., Sánchez-Reyes, J.M. et al. Relationship between episodic memory and volume of the brain regions of two functional cortical memory systems in multiple sclerosis. J Neurol 265, 2182–2189 (2018). https://doi.org/10.1007/s00415-018-8965-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-018-8965-x

Keywords

Search

Navigation