Dementia and Neurocognitive Disorders (대한치매학회지)

Korean Dementia Association (대한치매학회)
권호 표지
DOI QR코드

DOI QR Code

Facial Emotion Recognition in Older Adults With Cognitive Complaints

  • YongSoo Shim (Department of Neurology, The Catholic University of Korea, Eunpyeong St. Mary's Hospital)
  • Received : 2023.10.05
  • Accepted : 2023.11.01
  • Published : 2023.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

Background and Purpose: Facial emotion recognition deficits impact the daily life, particularly of Alzheimer's disease patients. We aimed to assess these deficits in the following three groups: subjective cognitive decline (SCD), mild cognitive impairment (MCI), and mild Alzheimer's dementia (AD). Additionally, we explored the associations between facial emotion recognition and cognitive performance. Methods: We used the Korean version of the Florida Facial Affect Battery (K-FAB) in 72 SCD, 76 MCI, and 76 mild AD subjects. The comparison was conducted using the analysis of covariance (ANCOVA), with adjustments being made for age and sex. The Mini-Mental State Examination (MMSE) was utilized to gauge the overall cognitive status, while the Seoul Neuropsychological Screening Battery (SNSB) was employed to evaluate the performance in the following five cognitive domains: attention, language, visuospatial abilities, memory, and frontal executive functions. Results: The ANCOVA results showed significant differences in K-FAB subtests 3, 4, and 5 (p=0.001, p=0.003, and p=0.004, respectively), especially for anger and fearful emotions. Recognition of 'anger' in the FAB subtest 5 declined from SCD to MCI to mild AD. Correlations were observed with age and education, and after controlling for these factors, MMSE and frontal executive function were associated with FAB tests, particularly in the FAB subtest 5 (r=0.507, p<0.001 and r=-0.288, p=0.026, respectively). Conclusions: Emotion recognition deficits worsened from SCD to MCI to mild AD, especially for negative emotions. Complex tasks, such as matching, selection, and naming, showed greater deficits, with a connection to cognitive impairment, especially frontal executive dysfunction.

Keywords

Acknowledgement

This study was supported partly by the Institute of Clinical Medical Research of Eunpyeong St. Mary's Hospital, Research Fund, 2022.

References

  1. Kumfor F, Sapey-Triomphe LA, Leyton CE, Burrell JR, Hodges JR, Piguet O. Degradation of emotion processing ability in corticobasal syndrome and Alzheimer's disease. Brain 2014;137:3061-3072. 
  2. Vandekerckhove M, Plessers M, Van Mieghem A, Beeckmans K, Van Acker F, Maex R, et al. Impaired facial emotion recognition in patients with ventromedial prefrontal hypoperfusion. Neuropsychology 2014;28:605-612. 
  3. Hargrave R, Maddock RJ, Stone V. Impaired recognition of facial expressions of emotion in Alzheimer's disease. J Neuropsychiatry Clin Neurosci 2002;14:64-71. 
  4. Burnham H, Hogervorst E. Recognition of facial expressions of emotion by patients with dementia of the Alzheimer type. Dement Geriatr Cogn Disord 2004;18:75-79. 
  5. Kohler CG, Anselmo-Gallagher G, Bilker W, Karlawish J, Gur RE, Clark CM. Emotion-discrimination deficits in mild Alzheimer disease. Am J Geriatr Psychiatry 2005;13:926-933. 
  6. Lavenu I, Pasquier F. Perception of emotion on faces in frontotemporal dementia and Alzheimer's disease: a longitudinal study. Dement Geriatr Cogn Disord 2005;19:37-41. 
  7. Shimokawa A, Yatomi N, Anamizu S, Torii S, Isono H, Sugai Y, et al. Influence of deteriorating ability of emotional comprehension on interpersonal behavior in Alzheimer-type dementia. Brain Cogn 2001;47:423-433. 
  8. Adolphs R. How do we know the minds of others? Domain-specificity, simulation, and enactive social cognition. Brain Res 2006;1079:25-35. 
  9. Ganguli M, Blacker D, Blazer DG, Grant I, Jeste DV, Paulsen JS, et al. Classification of neurocognitive disorders in DSM-5: a work in progress. Am J Geriatr Psychiatry 2011;19:205-210. 
  10. Albert MS, Cohen C, Koff E. Perception of affect in patients with dementia of the Alzheimer type. Arch Neurol 1991;48:791-795. 
  11. Adolphs R. Neural systems for recognizing emotion. Curr Opin Neurobiol 2002;12:169-177. 
  12. Teng E, Lu PH, Cummings JL. Deficits in facial emotion processing in mild cognitive impairment. Dement Geriatr Cogn Disord 2007;23:271-279. 
  13. Ahn BY, Oh JH, Jo MK, Na DL, Kim EJ. Poster session. The validity and reliability of the Korean version of Florida facial affect battery: a preliminary study. In: Proceedings of the Korean Neurological Association; Seoul, Korea; 2009.
  14. Jack CR Jr, Petersen RC, Xu YC, Waring SC, O'Brien PC, Tangalos EG, et al. Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology 1997;49:786-794. 
  15. Haroutunian V, Purohit DP, Perl DP, Marin D, Khan K, Lantz M, et al. Neurofibrillary tangles in nondemented elderly subjects and mild Alzheimer disease. Arch Neurol 1999;56:713-718. 
  16. Goransson LG, Brun JG, Harboe E, Mellgren SI, Omdal R. Intraepidermal nerve fiber densities in chronic inflammatory autoimmune diseases. Arch Neurol 2006;63:1410-1413. 
  17. Korf ES, Wahlund LO, Visser PJ, Scheltens P. Medial temporal lobe atrophy on MRI predicts dementia in patients with mild cognitive impairment. Neurology 2004;63:94-100. 
  18. Geroldi C, Rossi R, Calvagna C, Testa C, Bresciani L, Binetti G, et al. Medial temporal atrophy but not memory deficit predicts progression to dementia in patients with mild cognitive impairment. J Neurol Neurosurg Psychiatry 2006;77:1219-1222.
  19. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, et al. The diagnosis of dementia due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011;7:263-269. 
  20. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011;7:270-279. 
  21. Jessen F, Amariglio RE, van Boxtel M, Breteler M, Ceccaldi M, Chetelat G, et al. A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer's disease. Alzheimers Dement 2014;10:844-852. 
  22. Morris JC. The clinical dementia rating (CDR): current version and scoring rules. Neurology 1993;43:2412-2414. 
  23. Folstein MF, Folstein SE, McHugh PR. "Mini-Mental State". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189-198. 
  24. Baek MJ, Kim K, Park YH, Kim S. The validity and reliability of the Mini-Mental State Examination-2 for detecting mild cognitive impairment and Alzheimer's disease in a Korean population. PLoS One 2016;11:e0163792. 
  25. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, et al. Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 1982-1983;17:37-49. 
  26. Ryu HJ, Yang DW. The Seoul Neuropsychological Screening Battery (SNSB) for comprehensive neuropsychological assessment. Dement Neurocogn Disord 2023;22:1-15. 
  27. Erkinjuntti T. Subcortical ischemic vascular disease and dementia. Int Psychogeriatr 2003;15 Suppl 1:23-26. 
  28. Bowers D, Blonder L, Heilman K. Florida Affect Battery. Gainesville: Center for Neuropsychological Studies, Department of Neurology, University of Florida, 1998.
  29. Anderson AK, Christoff K, Panitz D, De Rosa E, Gabrieli JD. Neural correlates of the automatic processing of threat facial signals. J Neurosci 2003;23:5627-5633. 
  30. Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, et al. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 1996;383:812-815. 
  31. Hariri AR, Mattay VS, Tessitore A, Fera F, Weinberger DR. Neocortical modulation of the amygdala response to fearful stimuli. Biol Psychiatry 2003;53:494-501. 
  32. Whalen PJ, Kagan J, Cook RG, Davis FC, Kim H, Polis S, et al. Human amygdala responsivity to masked fearful eye whites. Science 2004;306:2061. 
  33. Cahill L, McGaugh JL. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 1998;21:294-299. 
  34. Phelps EA. Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 2004;14:198-202. 
  35. Stork O, Pape HC. Fear memory and the amygdala: insights from a molecular perspective. Cell Tissue Res 2002;310:271-277. 
  36. Schneider LS. Cholinergic deficiency in Alzheimer's disease. pathogenic model. Am J Geriatr Psychiatry 1998;6:S49-S55.
  37. Shinotoh H, Fukushi K, Nagatsuka S, Tanaka N, Aotsuka A, Ota T, et al. The amygdala and Alzheimer's disease: positron emission tomographic study of the cholinergic system. Ann N Y Acad Sci 2003;985:411-419.
  38. Emery NJ, Amaral DG. The role of the amygdala in primate social cognition. In: Cognitive Neuroscience of Emotion. New York: Oxford University Press, 2000;156-191.
  39. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 1995;269:1115-1118. 
  40. Adolphs R, Tranel D, Damasio H, Damasio A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 1994;372:669-672. 
  41. Kumfor F, Irish M, Hodges JR, Piguet O. Discrete neural correlates for the recognition of negative emotions: insights from frontotemporal dementia. PLoS One 2013;8:e67457. 
  42. Scott SK, Young AW, Calder AJ, Hellawell DJ, Aggleton JP, Johnson M. Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature 1997;385:254-257. 
  43. Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Barrett LF. The brain basis of emotion: a metaanalytic review. Behav Brain Sci 2012;35:121-143. 
  44. Abbott JD, Cumming G, Fidler F, Lindell AK. The perception of positive and negative facial expressions in unilateral brain-damaged patients: a meta-analysis. Laterality 2013;18:437-459. 
  45. Bora E, Meletti S. Social cognition in temporal lobe epilepsy: a systematic review and meta-analysis. Epilepsy Behav 2016;60:50-57. 
  46. Bora E, Velakoulis D, Walterfang M. Social cognition in Huntington's disease: a meta-analysis. Behav Brain Res 2016;297:131-140. 
  47. Coundouris SP, Adams AG, Henry JD. Empathy and theory of mind in Parkinson's disease: a metaanalysis. Neurosci Biobehav Rev 2020;109:92-102. 
  48. Rosenberg H, McDonald S, Dethier M, Kessels RP, Westbrook RF. Facial emotion recognition deficits following moderate-severe traumatic brain injury (TBI): re-examining the valence effect and the role of emotion intensity. J Int Neuropsychol Soc 2014;20:994-1003. 
  49. Anderson AK, Phelps EA. Expression without recognition: contributions of the human amygdala to emotional communication. Psychol Sci 2000;11:106-111. 
  50. Henry JD, von Hippel W, Molenberghs P, Lee T, Sachdev PS. Clinical assessment of social cognitive function in neurological disorders. Nat Rev Neurol 2016;12:28-39.