Advertisement

Journal of Neurology

, Volume 262, Issue 7, pp 1681–1690 | Cite as

Executive dysfunction predicts social cognition impairment in amyotrophic lateral sclerosis

  • Tamlyn J. Watermeyer
  • Richard G. Brown
  • Katie C. L. Sidle
  • David J. Oliver
  • Christopher Allen
  • Joanna Karlsson
  • Catherine M. Ellis
  • Christopher E. Shaw
  • Ammar Al-Chalabi
  • Laura H. Goldstein
Original Communication

Abstract

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder of the motor system with recognised extra-motor and cognitive involvement. This cross-sectional study examined ALS patients’ performance on measures requiring social inference, and determined the relationship between such changes and variations in mood, behaviour, personality, empathy and executive function. Fifty-five ALS patients and 49 healthy controls were compared on tasks measuring social cognition and executive function. ALS patients also completed measures examining mood, behaviour and personality. Regression analyses explored the contribution of executive function, mood, behaviour and personality to social cognition scores within the ALS sample. A between-group MANOVA revealed that, the ALS group was impaired relative to controls on two composite scores for social cognition and executive function. Patients also performed worse on individual tests of executive function measuring cognitive flexibility, response inhibition and concept formation, and on individual aspects of social cognition assessing the attribution of emotional and mental states. Regression analyses indicated that ALS-related executive dysfunction was the main predictor of social cognition performance, above and beyond demographic variables, behaviour, mood and personality. On at least some aspects of social cognition, impaired performance in ALS appears to be secondary to executive dysfunction. The profile of cognitive impairment in ALS supports a cognitive continuum between ALS and frontotemporal dementia.

Keywords

Motor neuron disease Executive function Social cognition Dementia 

Notes

Acknowledgments

We thank the patients with ALS who participated in the research. In addition to the listed authors, we thank the following individuals who made a significant contribution to the work reported in this paper: Dr Rachael Burman; Catherine Knights; Andrew Dougherty; Dr Naomi Martin; Rachel Tuck; Dr Robin Howard; Jan Clarke; Christine Batts; Hazel Watts; Joanna Sasson; Helen Copesy; Trish Cutts; Lucy Adamzyck. This study was funded by the Medical Research Council; The National Institute of Health Research (NIHR) Dementias and Neurodegenerative Diseases Research Network; the Motor Neurone Disease Association. The work leading up to this publication was funded by the European Community’s Health Seventh Framework Programme (AAC & CES, grant number 259867). AAC & CES are involved in two EU Joint Programmes—Neurodegenerative Disease Research (JPND) projects (STRENGTH and ALS-CarE). These projects are supported through the following funding organisations under the aegis of JPND—www.jpnd.eu: United Kingdom, Medical Research Council and Economic and Social Research Council. RGB, AAC, CES and LHG receive salary support from the NIHR Dementia Biomedical Research Unit and/or the NIHR Biomedical Research Centre for Mental Health, both at the South London and Maudsley NHS Foundation Trust and King’s College London. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health.

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical standard

Ethics approval was obtained from the National Research Ethics South East London Research Ethics Committee 4 (11/H0807/1). Informed written consent was obtained from all participants. Ethical standards were consistent with the 1964 Declaration of Helsinki and its later amendments.

Supplementary material

415_2015_7761_MOESM1_ESM.pdf (288 kb)
Supplementary material 1 (PDF 287 kb)

References

  1. 1.
    Goldstein LH, Abrahams S (2013) Changes in cognition and behaviour in amyotrophic lateral sclerosis: nature of impairment and implications for assessment. Lancet Neurol 12:368–380. doi: 10.1016/S1474-4422(13)70026-7 CrossRefPubMedGoogle Scholar
  2. 2.
    Lillo P, Savage S, Mioshi E et al (2012) Amyotrophic lateral sclerosis and frontotemporal dementia: a behavioural and cognitive continuum. Amyotroph Lateral Scler 13:102–109. doi: 10.3109/17482968.2011.639376 CrossRefPubMedGoogle Scholar
  3. 3.
    Lillo P, Mioshi E, Burrell JR et al (2012) Grey and white matter changes across the amyotrophic lateral sclerosis-frontotemporal dementia continuum. PLoS One 7:e43993. doi: 10.1371/journal.pone.0043993 PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Raaphorst J, de Visser M, Linssen WH et al (2010) The cognitive profile of amyotrophic lateral sclerosis: a meta-analysis. Amyotroph Lateral Scler 11:27–37. doi: 10.3109/17482960802645008 CrossRefPubMedGoogle Scholar
  5. 5.
    Taylor LJ, Brown RG, Tsermentseli S et al (2013) Is language impairment more common than executive dysfunction in amyotrophic lateral sclerosis? J Neurol Neurosurg Psychiatry 84:494–498. doi: 10.1136/jnnp-2012-303526 CrossRefPubMedGoogle Scholar
  6. 6.
    Witgert M, Salamone AR, Strutt AM et al (2010) Frontal-lobe mediated behavioural dysfunction in amyotrophic lateral sclerosis. Eur J Neurol 17:103–110. doi: 10.1111/j.1468-1331.2009.02801.x CrossRefPubMedGoogle Scholar
  7. 7.
    Grossman AB, Levin BE, Bradley WG (2006) Premorbid personality characteristics of patients with ALS. Amyotroph Lateral Scler 7:27–31. doi: 10.1080/14660820510012004 CrossRefPubMedGoogle Scholar
  8. 8.
    Beer JS, Ochsner KN (2006) Social cognition: a multi level analysis. Brain Res 1079:98–105. doi: 10.1016/j.brainres.2006.01.002 CrossRefPubMedGoogle Scholar
  9. 9.
    Adolphs R (2009) The social brain: neural basis of social knowledge. Annu Rev Psychol 60:693–716. doi: 10.1146/annurev.psych.60.110707.163514 PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Elamin M, Pender N, Hardiman O et al (2012) Social cognition in neurodegenerative disorders: a systematic review. J Neurol Neurosurg Psychiatry 83:1071–1079. doi: 10.1136/jnnp-2012-302817 CrossRefPubMedGoogle Scholar
  11. 11.
    Baron-Cohen S, Frith U (1985) Does the autistic child have a “theory of mind”? Cognition 21:37–46. doi: 10.1016/0010-0277(85)90022-8 CrossRefPubMedGoogle Scholar
  12. 12.
    Zimmerman EK, Eslinger PJ, Simmons Z et al (2007) Emotional perception deficits in amyotrophic lateral sclerosis. Cogn Behav Neurol 20:79–82. doi: 10.1097/WNN.0b013e31804c700b CrossRefPubMedGoogle Scholar
  13. 13.
    Girardi A, MacPherson SE, Abrahams S (2011) Deficits in emotional and social cognition in amyotrophic lateral sclerosis. Neuropsychology 25:53–65. doi: 10.1037/a0020357 CrossRefPubMedGoogle Scholar
  14. 14.
    Papps B, Abrahams S, Wicks P, Leigh PN, Goldstein LH (2005) Changes in memory for emotional material in amyotrophic lateral sclerosis (ALS). Neuropsychologia 43:1107–1114. doi: 10.1016/j.neuropsychologia.2004.11.027 CrossRefPubMedGoogle Scholar
  15. 15.
    Staios M, Fisher F, Lindell AK et al (2013) Exploring sarcasm detection in amyotrophic lateral sclerosis using ecologically valid measures. Front Hum Neurosci 7:178. doi: 10.3389/fnhum.2013.00178 PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    Savage SA, Lillo P, Kumfor F et al (2014) Emotion processing deficits distinguish pure amyotrophic lateral sclerosis from frontotemporal dementia. Amyotroph Lateral Scler Frontotemporal Degener 15:39–46. doi: 10.3109/21678421.2013.809763 CrossRefPubMedGoogle Scholar
  17. 17.
    Abrahams S (2011) Social cognition in amyotrophic lateral sclerosis. Neurodegener Dis Manag 1:397–405. doi: 10.2217/nmt.11.54 CrossRefGoogle Scholar
  18. 18.
    Gibbons Z, Snowden JS, Thompson JC et al (2007) Inferring thought and action in motor neurone disease. Neuropsychologia 45:1196–1207. doi: 10.1016/j.neuropsychologia.2006.10.008 CrossRefPubMedGoogle Scholar
  19. 19.
    Cerami C, Dodich A, Canessa N et al (2013) Emotional empathy in amyotrophic lateral sclerosis: a behavioural and voxel-based morphometry study. Amyotroph Lateral Scler Frontotemporal Degener 15:21–29. doi: 10.3109/21678421.2013.785568 CrossRefPubMedGoogle Scholar
  20. 20.
    Meier SL, Charleston AJ, Tippett LJ (2010) Cognitive and behavioural deficits associated with the orbitomedial prefrontal cortex in amyotrophic lateral sclerosis. Brain 133:3444–3457. doi: 10.1093/brain/awq254 CrossRefPubMedGoogle Scholar
  21. 21.
    van der Hulst E-J, Bak TH, Abrahams S (2014) Impaired affective and cognitive theory of mind and behavioural change in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. doi: 10.1136/jnnp-2014-309290 (Published online first: 4 Dec 2014) PubMedGoogle Scholar
  22. 22.
    Cavallo M, Adenzato M, Macpherson SE et al (2011) Evidence of social understanding impairment in patients with amyotrophic lateral sclerosis. PLoS One 6:e25948. doi: 10.1371/journal.pone.0025948 PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Brooks BR, Miller RG, Swash M et al (2000) World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1:293–299. doi: 10.1080/146608200300079536 CrossRefPubMedGoogle Scholar
  24. 24.
    Johns MW (1991) A new method for measuring daytime sleepiness: the Epworth Sleepiness Scale. Sleep 14:540–545PubMedGoogle Scholar
  25. 25.
    Holdnack J (2001) Wechsler test of adult reading. Psychological corporation, San AntonioGoogle Scholar
  26. 26.
    Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence. Psychological corporation, San AntonioGoogle Scholar
  27. 27.
    Gibbons CJ, Mills RJ, Thornton EW et al (2011) Rasch analysis of the Hospital Anxiety and Depression Scale (HADS) for use in motor neurone disease. Health Qual Life Outcomes 9:82. doi: 10.1186/1477-7525-9-82 PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    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. doi: 10.1016/S0022-510X(99)00210-5 CrossRefPubMedGoogle Scholar
  29. 29.
    Baron-Cohen S, Wheelwright S, Hill J et al (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. doi: 10.1111/1469-7610.00715 CrossRefPubMedGoogle Scholar
  30. 30.
    McDonald S, Flanagan S, Rollins JB (2002) The awareness of social inference test (TASIT). Thames valley test company, Bury St EdmondsGoogle Scholar
  31. 31.
    Happé F, Brownell H, Winner E (1999) Acquired ‘theory of mind’ impairments following stroke. Cognition 70:211–240. doi: 10.1016/S0010-0277(99)00005-0 CrossRefPubMedGoogle Scholar
  32. 32.
    Delis D, Kaplan E, Krammer J (2001) Delis—kaplan executive function system. Psychological corporation, San AntonioGoogle Scholar
  33. 33.
    Abrahams S, Leigh PN, Harvey A et al (2000) Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia 38:734–747. doi: 10.1016/S0028-3932(99)00146-3 CrossRefPubMedGoogle Scholar
  34. 34.
    Burgess PW, Shallice T (1997) The Hayling and Brixton tests. Thames valley company, Bury St EdmondsGoogle Scholar
  35. 35.
    Grace J, Malloy P (2001) Frontal Systems Behavioural scale (FrSBe). Psychological assessment resources Inc, FloridaGoogle Scholar
  36. 36.
    Davis M (1980) A multidimensional approach to individual differences in empathy. JSAS Cat Sel Doc Psycholo 10:113–126. doi: 10.1037/0022-3514.44.1.113 Google Scholar
  37. 37.
    Newsom-Davis IC, Abrahams S, Goldstein LH, Leigh PN (1999) The Emotional Lability Questionnaire: a new measure of emotional lability in amyotrophic lateral sclerosis. J Neurol Sci 169:22–25CrossRefPubMedGoogle Scholar
  38. 38.
    Costa PT, McCrae RR (1992) The Revised NEO Personal Inventory (NEO PI-R) and NEO Five-Factor Inventory (NEO-FFI) Professional Manual. Psychological assessment resources Inc, FloridaGoogle Scholar
  39. 39.
    Leys C, Ley C, Klein O et al (2013) Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the median. J Exp Soc Psychol 49:764–766. doi: 10.1016/j.jesp.2013.03.013 CrossRefGoogle Scholar
  40. 40.
    D’Agostino RB, Belanger A, D’Agostino RB Jr (1990) A suggestion for using powerful and informative tests of normality. Am Stat 44:316–321. doi: 10.2307/2684359 Google Scholar
  41. 41.
    Royston JP (1983) Some techniques for assessing multivariate normality based on the Shapiro–Wilk w. Appl Stat J Roy STC 32:121–133. doi: 10.2307/2347291 Google Scholar
  42. 42.
    R Core Team (2015) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna. http://www.R-project.org/
  43. 43.
    IBM Corp. Released 2012. IBM SPSS statistics for windows, Version 21.0. IBM Corp, ArmonkGoogle Scholar
  44. 44.
    Strong MJ, Grace GM, Freedman M et al (2009) Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 10:131–146. doi: 10.1080/17482960802654364 CrossRefPubMedGoogle Scholar
  45. 45.
    Snowden JS, Austin NA, Sembi S et al (2008) Emotion recognition in Huntington’s disease and frontotemporal dementia. Neuropsychologia 46:2638–2649. doi: 10.1016/j.neuropsychologia.2008.04.018 CrossRefPubMedGoogle Scholar
  46. 46.
    Rascovsky K, Hodges JR, Kipps CM et al (2007) Diagnostic criteria for the behavioural variant of frontotemporal dementia (bvFTD): current limitations and future directions. Alzheimer Dis Assoc Disord 21:S14–S18. doi: 10.1097/WAD.0b013e31815c3445 CrossRefPubMedGoogle Scholar
  47. 47.
    Eslinger PJ, Moore P, Anderson C et al (2011) Social cognition, executive functioning, and neuroimaging correlates of empathic deficits in frontotemporal dementia. J Neuropsychiatry Clin Neurosci 23:74–82. doi: 10.1176/jnp.23.1.jnp74 PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Kipps CM, Nestor PJ, Acosta-Cabronero J et al (2009) Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing. Brain 132:592–603. doi: 10.1093/brain/awn314 CrossRefPubMedGoogle Scholar
  49. 49.
    McCrae R, John O (1992) An introduction to the five-factor model and its applications. J Pers 60:175–215. doi: 10.1111/j.1467-6494.1992.tb00970.x CrossRefPubMedGoogle Scholar
  50. 50.
    Martin I, McDonald S (2003) Weak coherence, no theory of mind, or executive dysfunction? Solving the puzzle of pragmatic language disorders. Brain Lang 85:451–466. doi: 10.1016/S0093-934X(03)00070-1 CrossRefPubMedGoogle Scholar
  51. 51.
    Kaiser NC, Lee GJ, Lu PH et al (2013) What dementia reveals about proverb interpretation and its neuroanatomical correlates. Neuropsychologia 51:1726–1733. doi: 10.1016/j.neuropsychologia.2013.05.021 CrossRefPubMedGoogle Scholar
  52. 52.
    Papagno C, Genoni A (2004) The role of syntactic competence in idiom comprehension: a study on aphasic patients. J Neurolinguistics 17:371–382. doi: 10.1016/j.jneuroling.2003.11.002 CrossRefGoogle Scholar
  53. 53.
    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. doi: 10.3109/21678421.2013.805784 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Tamlyn J. Watermeyer
    • 1
  • Richard G. Brown
    • 2
  • Katie C. L. Sidle
    • 3
  • David J. Oliver
    • 4
    • 5
  • Christopher Allen
    • 6
  • Joanna Karlsson
    • 7
  • Catherine M. Ellis
    • 8
  • Christopher E. Shaw
    • 9
  • Ammar Al-Chalabi
    • 9
  • Laura H. Goldstein
    • 2
  1. 1.Department of PsychologyBangor UniversityBangorUK
  2. 2.Department of Psychology, PO77, Henry Wellcome Building, Institute of Psychiatry, Psychology and NeuroscienceKing’s College LondonLondonUK
  3. 3.Department of Molecular Neuroscience, Institute of NeurologyUniversity College LondonLondonUK
  4. 4.Medway Community Healthcare TrustThe Wisdom HospiceKentUK
  5. 5.The Centre for Professional PracticeUniversity of KentKentUK
  6. 6.Addenbrooke’s Motor Neuron Disease Care and Research CentreCambridge University Hospitals NHS TrustCambridgeUK
  7. 7.East Kent Motor Neurone Disease ServiceEast Kent Hospitals University NHS TrustKentUK
  8. 8.Motor Nerve Clinic, Academic Neurosciences CentreKing’s College Hospital NHS Foundation TrustLondonUK
  9. 9.Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and NeuroscienceKing’s College LondonLondonUK

Personalised recommendations