Skip to main content

Advertisement

SpringerLink
Log in

Reading the mind in the eyes in patients with idiopathic REM sleep behavior disorder

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Objectives

Idiopathic rapid eye movement (REM) sleep behavior disorder (iRBD) is characterized by vocalizations, jerks, and motor behaviors during REM sleep, often associated with REM-related dream content, which is considered a prodromal stage of α-synucleinopathy. The results of the Reading the Mind in the Eyes (RME) reflecting affective Theory of Mind (ToM) are inconsistent in α-synucleinopathy. The present study tried to investigate the RME in patients with iRBD.

Methods

A total of 35 patients with iRBD and 26 healthy controls were included in the study. All participants were administered the RME and the cognitive assessments according to a standard procedure. The patients with iRBD were further divided into two groups (high or low RME) according to the scores of the RME (> 21, or ≤ 20).

Results

The patients with iRBD had worse scores on cognitive tests compared with healthy controls involving global cognitive screening, memory, and visuospatial abilities (p < 0.05), but the scores of the RME were similar between the two groups (20.83 ± 3.38, 20.58 ± 3.43) (p ˃ 0.05). Patients with low RME had more obvious cognitive impairments than healthy controls. After applying Bonferroni correction for multiple tests, the low REM group only performed worse on the Sum of trials 1 to 5 and delayed recall of the RAVLT compared with the healthy control group (p < 0.001, = 0.002). The RME correlated with the scores of cognitive tests involving executive function, attention, memory, and visuospatial function.

Conclusions

The changes in RME had a relationship with cognitive impairments, especially memory, in patients with iRBD.

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

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Högl B, Stefani A, Videnovic A (2018) Idiopathic REM sleep behaviour disorder and neurodegeneration-an update. Nat Rev Neurol 14:40–55. https://doi.org/10.1038/nrneurol.2017.157

    Article  PubMed  Google Scholar 

  2. Cicero CE, Giuliano L, Luna J, Zappia M, Preux PM, Nicoletti A (2021) Prevalence of idiopathic REM behavior disorder: a systematic review and meta-analysis. Sleep 44:zsaa294. https://doi.org/10.1093/sleep/zsaa294

    Article  PubMed  Google Scholar 

  3. Stang CD, Mullan AF, Hajeb M, Camerucci E, Turcano P, Martin P et al (2021) Timeline of Rapid eye movement sleep behavior disorder in overt alpha-synucleinopathies. Ann Neurol 89:293–303. https://doi.org/10.1002/ana.25952

    Article  CAS  PubMed  Google Scholar 

  4. Galbiati A, Verga L, Giora E, Zucconi M, Ferini-Strambi L (2019) The risk of neurodegeneration in REM sleep behavior disorder: a systematic review and meta-analysis of longitudinal studies. Sleep Med Rev 43:37–46. https://doi.org/10.1016/j.smrv.2018.09.008

    Article  PubMed  Google Scholar 

  5. Carli G, Caminiti SP, Sala A, Galbiati A, Pilotto A, Ferini-Strambi L et al (2020) Impaired metabolic brain networks associated with neurotransmission systems in the α-synuclein spectrum. Parkinsonism Relat Disord 81:113–122. https://doi.org/10.1016/j.parkreldis.2020.10.036

    Article  PubMed  Google Scholar 

  6. Pinkham AE, Penn DL, Green MF, Buck B, Healey K, Harvey PD (2014) The social cognition psychometric evaluation study: results of the expert survey and RAND panel. Schizophr Bull 40:813–823. https://doi.org/10.1093/schbul/sbt081

    Article  PubMed  Google Scholar 

  7. Henry JD, von Hippel W, Molenberghs P, Lee T, Sachdev PS (2016) Clinical assessment of social cognitive function in neurological disorders. Nat Rev Neurol 12:28–39. https://doi.org/10.1038/nrneurol.2015.229

    Article  PubMed  Google Scholar 

  8. Poletti M, Enrici I, Adenzato M (2012) Cognitive and affective theory of mind in neurodegenerative diseases: neuropsychological, neuroanatomical and neurochemical levels. Neurosci Biobehav Rev 36:2147–2164. https://doi.org/10.1016/j.neubiorev.2012.07.004

    Article  PubMed  Google Scholar 

  9. Stewart E, Catroppa C, Lah S (2016) Theory of mind in patients with epilepsy: a systematic review and meta-analysis. Neuropsychol Rev 26:3–24. https://doi.org/10.1007/s11065-015-9313-x

    Article  PubMed  Google Scholar 

  10. Olderbak S, Wilhelm O, Olaru G, Geiger M, Brenneman MW, Roberts RD (2015) A psychometric analysis of the reading the mind in the eyes test: toward a brief form for research and applied settings. Front Psychol 6:1503. https://doi.org/10.3389/fpsyg.2015.01503

    Article  PubMed  PubMed Central  Google Scholar 

  11. American Academy of Sleep Medicine (2015) The international classification of sleep disorders, 2nd edn. American Academy of Sleep Medicine, Westchester, pp 148–52

    Google Scholar 

  12. Zhang M, Katzman R, Salmon D, Jin H, Cai GJ, Wang ZY et al (1990) The prevalence of dementia and Alzheimer’s disease in Shanghai, China: impact of age, gender, and education. Ann Neurol 27:428–437. https://doi.org/10.1002/ana.410270412

    Article  CAS  PubMed  Google Scholar 

  13. Wang Y, Wang ZW, Yang YC, Wu HJ, Zhao HY, Zhao ZX (2015) Validation of the rapid eye movement sleep behavior disorder screening questionnaire in China. J Clin Neurosci 22:1420–1424. https://doi.org/10.1016/j.jocn.2015.03.008

    Article  PubMed  Google Scholar 

  14. Nasreddine Z, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I et al (2005) The Montreal Cognitive Assessment, MoCA: A brief screening tool for Mild Cognitive Impairment. J Am Geriatr Soc 53:695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.x

    Article  PubMed  Google Scholar 

  15. Dai XY, Ryan JJ, Paolo AM, Harrington RG (1990) Factor analysis of the mainland Chinese version of the Wechsler Adult Intelligence Scale (WAIS-RC) in a brain-damaged sample. Int J Neurosci 55:107–111. https://doi.org/10.3109/00207459008985956

    Article  CAS  PubMed  Google Scholar 

  16. Strauss E, Sherman EM, Spreen O (2006) A compendium of neuropsychological tests: administration, norms, and commentary, 3rd edn. Oxford University Press, New York

    Google Scholar 

  17. Osterrieth PA (1944) Le test de copie d’une figure complexe. Arch Psychol 30:206–356

    Google Scholar 

  18. Lu L, Bigler ED (2000) Performance on original and a Chinese version of trail making test part B: a normative bilingual sample. Appl Neuropsychol 7:243–246. https://doi.org/10.1207/S15324826AN0704_6

    Article  CAS  PubMed  Google Scholar 

  19. Cheung RW, Cheung MC, Chan AS (2004) Confrontation naming in Chinese patients with left, right or bilateral brain damage. J Int Neuropsychol Soc 10:46–53. https://doi.org/10.1017/S1355617704101069

    Article  PubMed  Google Scholar 

  20. Rouleau I, Salmon DP, Butters N, Kennedy C, McGuire K (1992) Quantitative and qualitative analyses of Clock Drawings in Alzheimer’s and Huntington’s Disease. Brain cogn 18:70–87. https://doi.org/10.1016/0278-2626(92)90112-y

    Article  CAS  PubMed  Google Scholar 

  21. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I (2001) The “Reading the Mind in the Eyes” test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry 42:241–251

    Article  CAS  PubMed  Google Scholar 

  22. Coundouris SP, Adams AG, Henry JD (2020) Empathy and theory of mind in Parkinson’s disease: a meta-analysis. Neurosci Biobehav Rev 109:92–102. https://doi.org/10.1016/j.neubiorev.2019.12.030

    Article  PubMed  Google Scholar 

  23. Romosan AM, Dehelean L, Romosan RS, Andor M, Bredicean AC, Simu MA (2019) Affective theory of mind in Parkinson’s disease: the effect of cognitive performance. Neuropsychiatr Dis Treat 15:2521–2535. https://doi.org/10.2147/NDT.S219288

    Article  PubMed  PubMed Central  Google Scholar 

  24. Bora E, Walterfang M, Velakoulis D (2015) Theory of mind in Parkinson’s disease: a meta-analysis. Behav Brain Res 292:515–520. https://doi.org/10.1016/j.bbr.2015.07.012

    Article  PubMed  Google Scholar 

  25. Ferini-Strambi L, Fasiello E, Sforza M, Salsone M, Galbiati A (2019) Neuropsychological, electrophysiological, and neuroimaging biomarkers for REM behavior disorder. Expert Rev Neurother 19:1069–1087. https://doi.org/10.1080/14737175.2019.1640603

    Article  CAS  PubMed  Google Scholar 

  26. Li X, Zhou Z, Jia S, Hou C, Zheng W, Rong P et al (2016) Cognitive study on Chinese patients with idiopathic REM sleep behavior disorder. J Neurol Sci 366:82–86. https://doi.org/10.1016/j.jns.2016.04.047

    Article  PubMed  Google Scholar 

  27. Wenke Š, Mana J, Havlík F, Cohn M, Nikolai T, Buschke H et al (2022) Characterization of memory profile in idiopathic REM sleep behavior disorder. J Clin Exp Neuropsychol 44:237–250. https://doi.org/10.1080/13803395.2022.2107182

    Article  PubMed  Google Scholar 

  28. Heitz C, Noblet V, Phillipps C, Cretin B, Vogt N, Philippi N et al (2016) Cognitive and affective theory of mind in dementia with Lewy bodies and Alzheimer’s disease. Alzheimers Res Ther 8:10. https://doi.org/10.1186/s13195-016-0179-9

  29. Yi Z, Zhao P, Zhang H, Shi Y, Shi H, Zhong J et al (2020) Theory of mind in Alzheimer’s disease and amnestic mild cognitive impairment: a meta-analysis. Neurol Sci 41:1027–1039. https://doi.org/10.1007/s10072-019-04215-5

    Article  PubMed  Google Scholar 

  30. Yildirim E, Soncu Buyukiscan E, Demirtas-Tatlidede A, Bilgiç B, Gurvit H (2020) An investigation of affective theory of mind ability and its relation to neuropsychological functions in Alzheimer’s disease. J Neuropsychol 14:399–415. https://doi.org/10.1111/jnp.12207

    Article  PubMed  Google Scholar 

  31. Morellini L, Izzo A, Ceroni M, Rossi S, Zerboni G, Rege-Colet L et al (2022) Theory of mind in patients with mild cognitive impairment: a systematic review. Front Psychol 13:994070. https://doi.org/10.3389/fpsyg.2022.994070

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rossetto F, Isernia S, Cabinio M, Pirastru A, Blasi V, Baglio F (2022) Affective theory of mind as a residual ability to preserve mentalizing in amnestic mild cognitive impairment: a 12-months longitudinal study. Front Neurol 13:1060699. https://doi.org/10.3389/fneur.2022.1060699

    Article  PubMed  PubMed Central  Google Scholar 

  33. Génier Marchand D, Montplaisir J, Postuma RB, Rahayel S, Gagnon JF (2017) Detecting the cognitive prodrome of dementia with Lewy bodies: a prospective study of REM sleep behavior disorder. Sleep 40:1–11. https://doi.org/10.1093/sleep/zsw014

    Article  Google Scholar 

  34. Génier Marchand D, Postuma RB, Escudier F, De Roy J, Pelletier A, Montplaisir J et al (2018) How does dementia with Lewy bodies start? prodromal cognitive changes in REM sleep behavior disorder. Ann Neurol 83:1016–1026. https://doi.org/10.1002/ana.25239

    Article  PubMed  Google Scholar 

  35. Terzaghi M, Toscano G, Casoni F, Picascia M, Arnaldi D, Rustioni V et al (2019) Assessment of cognitive profile as a prodromal marker of the evolution of rapid eye movement sleep behavior disorder. Sleep 42:zsz103. https://doi.org/10.1093/sleep/zsz103

    Article  PubMed  Google Scholar 

  36. Postuma RB, Iranzo A, Hu M, Högl B, Boeve BF, Manni R et al (2019) Risk and predictors of dementia and parkinsonism in idiopathic REM sleep behaviour disorder: a multicentre study. Brain 142:744–759. https://doi.org/10.1093/brain/awz030

    Article  PubMed  PubMed Central  Google Scholar 

  37. Joza S, Hu MT, Jung KY, Kunz D, Arnaldi D, Lee JY et al (2023) International REM sleep behavior disorder study group prodromal dementia with Lewy bodies in REM sleep behavior disorder: a multicenter study. Alzheimer’s Dement 1–12. https://doi.org/10.1002/alz.13386

  38. Otsuka Y, Shizawa M, Sato A, Itakura S (2021) The role of executive functions in older adults’ affective theory of mind. Arch Gerontol Geriatr 97:104513. https://doi.org/10.1016/j.archger.2021.104513

    Article  PubMed  Google Scholar 

  39. Fastame MC, Carta V (2023) Do cognitive reserve and executive functions matter to perform the reading the mind in the eyes test in late lifespan? Appl Neuropsychol Adult 30:696–704. https://doi.org/10.1080/23279095.2021.1972422

  40. Nandrino JL, Gandolphe MC, Alexandre C, Kmiecik E, Yguel J, Urso L (2014) Cognitive and affective theory of mind abilities in alcohol-dependent patients: the role of autobiographical memory. Drug Alcohol Depend 143:65–73. https://doi.org/10.1016/j.drugalcdep.2014.07.010

    Article  PubMed  Google Scholar 

  41. Poletti M, Bonuccelli U (2013) Alteration of affective Theory of mind in amnestic mild cognitive impairment. J Neuropsychol 7:121–131. https://doi.org/10.1111/j.1748-6653.2012.02040.x

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by Key Projects of Strategic International Cooperation in Scientific and Technological Innovation in the National Key Research and Development Program (2018YFE0203600), Key Area in Research and Development Program of Guangdong Province (2018B030336001), and Personnel development funding projects of Beijing Dongcheng District (DCQYYRC-791–01-DR).

Author information

Authors and Affiliations

  1. Department of Cognitive Disorder, Beijing Tiantan Hospital, Capital Medical University, Fengtai District, South 4th Ring Road West 119, Beijing, 100070, China

    Xudong Li, Miaoxin Shen & Ziling Han

  2. China National Clinical Research Center for Neurological Diseases, Beijing, China

    Xudong Li

  3. ECG Room, She County Hospital, Handan, China

    Zhihong Shen

  4. Department of Neurology, China-Japan Friendship Hospital, Beijing, China

    Jinsong Jiao

  5. Department of Microbiology and Immunology, Medical School, Xizang Minzu University, Xianyang, China

    Xiaopeng Tong

Authors
  1. Xudong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miaoxin Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhihong Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ziling Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinsong Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaopeng Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xudong Li.

Ethics declarations

Ethics approval and consent to participate

The objectives of the research were explained to participants and their families, and written informed consent was obtained. The research was approved by the Ethics Committee of the Beijing Tiantan Hospital.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, X., Shen, M., Shen, Z. et al. Reading the mind in the eyes in patients with idiopathic REM sleep behavior disorder. Neurol Sci 45, 2697–2703 (2024). https://doi.org/10.1007/s10072-024-07303-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-024-07303-3

Keywords

Search

Navigation