J Clin Neurol.  2016 Jul;12(3):295-300. 10.3988/jcn.2016.12.3.295.

Impaired Perception of Emotional Expression in Amyotrophic Lateral Sclerosis

• Oh SI
• Oh KW
• Kim HJ
• Park JS
• Kim SH

• KMID: 2354116
• DOI: http://doi.org/10.3988/jcn.2016.12.3.295

Abstract

BACKGROUND AND PURPOSE
The increasing recognition that deficits in social emotions occur in amyotrophic lateral sclerosis (ALS) is helping to explain the spectrum of neuropsychological dysfunctions, thus supporting the view of ALS as a multisystem disorder involving neuropsychological deficits as well as motor deficits. The aim of this study was to characterize the emotion perception abilities of Korean patients with ALS based on the recognition of facial expressions.
METHODS
Twenty-four patients with ALS and 24 age- and sex-matched healthy controls completed neuropsychological tests and facial emotion recognition tasks [ChaeLee Korean Facial Expressions of Emotions (ChaeLee-E)]. The ChaeLee-E test includes facial expressions for seven emotions: happiness, sadness, anger, disgust, fear, surprise, and neutral.
RESULTS
The ability to perceive facial emotions was significantly worse among ALS patients performed than among healthy controls [65.2±18.0% vs. 77.1±6.6% (mean±SD), p=0.009]. Eight of the 24 patients (33%) scored below the 5th percentile score of controls for recognizing facial emotions.
CONCLUSIONS
Emotion perception deficits occur in Korean ALS patients, particularly regarding facial expressions of emotion. These findings expand the spectrum of cognitive and behavioral dysfunction associated with ALS into emotion processing dysfunction.

Keyword

amyotrophic lateral sclerosis; emotion; emotion perception; facial expression; frontotemporal dementia

MeSH Terms

Amyotrophic Lateral Sclerosis*
Anger
Facial Expression
Frontotemporal Dementia
Happiness
Humans
Neuropsychological Tests
Perception

Figure

• 

  Fig. 1 Distribution of scores on the ChaeLee Korean Facial Expressions of Emotions test between amyotrophic lateral sclerosis (ALS) patients and healthy controls.

Reference

1. Consonni M, Iannaccone S, Cerami C, Frasson P, Lacerenza M, Lunetta C, et al. The cognitive and behavioural profile of amyotrophic lateral sclerosis: application of the consensus criteria. Behav Neurol. 2013; 27:143–153.

2. Lillo P, Mioshi E, Burrell JR, Kiernan MC, Hodges JR, Hornberger M. Grey and white matter changes across the amyotrophic lateral sclerosis-frontotemporal dementia continuum. PLoS One. 2012; 7:e43993.

3. Oh SI, Park A, Kim HJ, Oh KW, Choi H, Kwon MJ, et al. Spectrum of cognitive impairment in Korean ALS patients without known genetic mutations. PLoS One. 2014; 9:e87163.

4. Phukan J, Pender NP, Hardiman O. Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurol. 2007; 6:994–1003.

5. Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH, et al. Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2009; 10:131–146.

6. Cerami C, Dodich A, Canessa N, Crespi C, Iannaccone S, Corbo M, et al. Emotional empathy in amyotrophic lateral sclerosis: a behavioural and voxel-based morphometry study. Amyotroph Lateral Scler Frontotemporal Degener. 2014; 15:21–29.

7. Lulé D, Kurt A, Jürgens R, Kassubek J, Diekmann V, Kraft E, et al. Emotional responding in amyotrophic lateral sclerosis. J Neurol. 2005; 252:1517–1524.

8. Savage SA, Lillo P, Kumfor F, Kiernan MC, Piguet O, Hodges JR. Emotion processing deficits distinguish pure amyotrophic lateral sclerosis from frontotemporal dementia. Amyotroph Lateral Scler Frontotemporal Degener. 2014; 15:39–46.

9. Zimmerman EK, Eslinger PJ, Simmons Z, Barrett AM. Emotional perception deficits in amyotrophic lateral sclerosis. Cogn Behav Neurol. 2007; 20:79–82.

10. Hornak J, Rolls ET, Wade D. Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia. 1996; 34:247–261.

11. Lillo P, Mioshi E, Hodges JR. Caregiver burden in amyotrophic lateral sclerosis is more dependent on patients' behavioral changes than physical disability: a comparative study. BMC Neurol. 2012; 12:156.

12. Roberts VJ, Ingram SM, Lamar M, Green RC. Prosody impairment and associated affective and behavioral disturbances in Alzheimer's disease. Neurology. 1996; 47:1482–1488.

13. Brooks BR, Miller RG, Swash M, Munsat TL. 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. 2000; 1:293–299.

14. Kimura F, Fujimura C, Ishida S, Nakajima H, Furutama D, Uehara H, et al. Progression rate of ALSFRS-R at time of diagnosis predicts survival time in ALS. Neurology. 2006; 66:265–267.

15. Gordon PH, Miller RG, Moore DH. ALSFRS-R. Amyotroph Lateral Scler Other Motor Neuron Disord. 2004; 5:Suppl 1. 90–93.

16. Han C, Jo SA, Jo I, Kim E, Park MH, Kang Y. An adaptation of the Korean mini-mental state examination (K-MMSE) in elderly Koreans: demographic influence and population-based norms (the AGE study). Arch Gerontol Geriatr. 2008; 47:302–310.

17. Jo SA, Park MH, Jo I, Ryu SH, Han C. Usefulness of Beck Depression Inventory (BDI) in the Korean elderly population. Int J Geriatr Psychiatry. 2007; 22:218–223.

18. Raaphorst J, Beeldman E, Jaeger B, Schmand B, van den Berg LH, Weikamp JG, et al. Is the Frontal Assessment Battery reliable in ALS patients? Amyotroph Lateral Scler Frontotemporal Degener. 2013; 14:73–74.

19. Lee KU, Kim J, Yeon B, Kim SH, Chae JH. Development and standardization of extended ChaeLee Korean facial expressions of emotions. Psychiatry Investig. 2013; 10:155–163.

20. Girardi A, Macpherson SE, Abrahams S. Deficits in emotional and social cognition in amyotrophic lateral sclerosis. Neuropsychology. 2011; 25:53–65.

21. Poletti M, Enrici I, Adenzato M. Cognitive and affective theory of mind in neurodegenerative diseases: neuropsychological, neuroanatomical and neurochemical levels. Neurosci Biobehav Rev. 2012; 36:2147–2164.

22. Kumfor F, Piguet O. Disturbance of emotion processing in frontotemporal dementia: a synthesis of cognitive and neuroimaging findings. Neuropsychol Rev. 2012; 22:280–297.

23. Keane J, Calder AJ, Hodges JR, Young AW. Face and emotion processing in frontal variant frontotemporal dementia. Neuropsychologia. 2002; 40:655–665.

24. Cavallo M, Adenzato M, Macpherson SE, Karwig G, Enrici I, Abrahams S. Evidence of social understanding impairment in patients with amyotrophic lateral sclerosis. PLoS One. 2011; 6:e25948.

25. Ahn SW, Kim SH, Kim JE, Kim SM, Kim SH, Sung JJ, et al. Frontal assessment battery to evaluate frontal lobe dysfunction in ALS patients. Can J Neurol Sci. 2011; 38:242–246.

26. Clark US, Neargarder S, Cronin-Golomb A. Specific impairments in the recognition of emotional facial expressions in Parkinson's disease. Neuropsychologia. 2008; 46:2300–2309.

27. Cuddy M, Papps BJ, Thambisetty M, Leigh PN, Goldstein LH. Processing and memory for emotional and neutral material in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2012; 13:592–598.

28. Kwon MJ, Baek W, Ki CS, Kim HY, Koh SH, Kim JW, et al. Screening of the SOD1, FUS, TARDBP, ANG, and OPTN mutations in Korean patients with familial and sporadic ALS. Neurobiol Aging. 2012; 33:1017.e17–1017.e23.

29. Renton AE, Chiò A, Traynor BJ. State of play in amyotrophic lateral sclerosis genetics. Nat Neurosci. 2014; 17:17–23.

30. Kim HS, Sasaki JY. Emotion regulation: the interplay of culture and genes. Soc Personal Psychol Compass. 2012; 6:865–877.

31. Adolphs R. Neural systems for recognizing emotion. Curr Opin Neurobiol. 2002; 12:169–177.

32. Crespi C, Cerami C, Dodich A, Canessa N, Arpone M, Iannaccone S, et al. Microstructural white matter correlates of emotion recognition impairment in amyotrophic lateral sclerosis. Cortex. 2014; 53:1–8.