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Journal of Neural Transmission

, Volume 125, Issue 12, pp 1819–1827 | Cite as

Emotional facedness in Parkinson’s disease

  • Lucia RicciardiEmail author
  • Federica Visco-Comandini
  • Roberto Erro
  • Francesca Morgante
  • Daniele Volpe
  • James Kilner
  • Mark J. Edwards
  • Matteo BolognaEmail author
Neurology and Preclinical Neurological Studies - Original Article

Abstract

People with Parkinson’s disease (PD) have a deficit of facial expression. Previous studies indicate that hemispheric dominance for emotional processing can give rise to an asymmetric pattern of facial expression of emotion. In this study, we aimed to evaluate possible asymmetry in facial emotion expressivity in PD. Twenty PD patients and twenty healthy controls were video-recorded while posing the 6 basic emotions. The most expressive pictures were derived from the videos and chimeric faces were created. Nine healthy raters were asked to judge which of the two chimeras looked more expressive. Chosen responses, reaction times and confidence levels were the main outcome measures. We evaluated possible differences in these measures within each group and between groups (PD, healthy controls). We assessed possible correlations between a global facial laterality index (pooling all emotions together) as well as facial laterality indexes for each emotion and the body laterality index, accounting for the predominant side of limb bradykinesia in patients. There was no difference in outcome measures when evaluating the two hemifaces within PD patients and healthy controls or between the two groups (all Ps > 0.05). In PD patients there was a correlation between the global facial laterality index and the body laterality index (R = − 0.39, P = 0.01), suggesting that the most expressive hemiface corresponded to the less affected body side. The results of our study do not support the hypothesis of hemisphere predominance in regulating facial emotion expressions and provides novel information on altered facial emotion expression in PD.

Keywords

Parkinson’s disease Emotion Laterality Asymmetry Expressivity 

Abbreviations

BDI

Beck depression inventory

CR

Chosen response

CL

Confidence level

HH

Hemi-hypomimia

HC

Healthy controls

LL

Left–left

LA

Less-affected

LEDD

Levodopa equivalent daily dose

MA

More-affected

MMSE

Mini mental state examination

PD

Parkinson’s disease

RT

Reaction time

RR

Right–right

Notes

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

References

  1. Argaud S, Delplanque S, Houvenaghel JF, Auffret M, Duprez J, Vérin M, Sauleau P (2016) Does facial amimia impact the recognition of facial emotions? An EMG study in Parkinson’s disease. PLoS One.  https://doi.org/10.1371/journal.pone.0160329 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Argaud S, Vérin M, Sauleau P, Grandjean D (2018) Facial emotion recognition in Parkinson’s disease: a review and new hypotheses. Mov Disord.  https://doi.org/10.1002/mds.27305 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baijal S, Srinivasan N (2011) Emotional and hemispheric asymmetries in shifts of attention: an ERP study. Cognit Emot 25(2):280–294.  https://doi.org/10.1080/02699931.2010.492719 CrossRefGoogle Scholar
  4. Bologna M, Fabbrini G, Marsili L, Defazio G, Thompson PD, Berardelli A (2013) Facial bradykinesia. J Neurol Neurosurg Psychiatry.  https://doi.org/10.1136/jnnp-2012-303993 CrossRefPubMedGoogle Scholar
  5. Bologna M, Berardelli I, Paparella G, Marsili L, Ricciardi L, Fabbrini G, Berardelli A (2016) Altered kinematics of facial emotion expression and emotion recognition deficits are unrelated in parkinson’s disease. Front Neurol.  https://doi.org/10.3389/fneur.2016.00230 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Borod JC, Koff E, Yecker S, Santschi C, Schmidt JM (1998) Facial asymmetry during emotional expression: gender, valence, and measurement technique. Neuropsychologia 36(11):1209–1215.  https://doi.org/10.1016/S0028-3932(97)00166-8 CrossRefPubMedGoogle Scholar
  7. Bowers D, Miller K, Bosch W, Gokcay D, Pedraza O, Springer U, Okun M (2006) Faces of emotion in Parkinsons disease: micro-expressivity and bradykinesia during voluntary facial expressions. J Int Neuropsychol Soc 12(6):765–773.  https://doi.org/10.1017/S135561770606111X CrossRefPubMedGoogle Scholar
  8. Cattaneo L, Pavesi G (2014) The facial motor system. Neurosci Biobehav Rev.  https://doi.org/10.1016/j.neubiorev.2013.11.002 CrossRefPubMedGoogle Scholar
  9. Crosiers D, MaréChal E, van Ael Y, Cras P (2011) Left-sided hemihypomimia in Parkinson’s disease. Acta Neurologica Belgica 111(3):225–227PubMedGoogle Scholar
  10. De Cock VC, Vidailhet M, Leu S, Texeira A, Apartis E, Elbaz A, Arnulf I (2007) Restoration of normal motor control in Parkinson’s disease during REM sleep. Brain 130(2):450–456.  https://doi.org/10.1093/brain/awl363 CrossRefPubMedGoogle Scholar
  11. Djaldetti R, Ziv I, Melamed E (2006) The mystery of motor asymmetry in Parkinson’s disease. Lancet Neurol 5(9):796–802.  https://doi.org/10.1016/S1474-4422(06)70549-X CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dolcos F, Rice HJ, Cabeza R (2002) Hemispheric asymmetry and aging: Right hemisphere decline or asymmetry reduction. Neurosci Biobehav Rev.  https://doi.org/10.1016/S0149-7634(02)00068-4 CrossRefPubMedGoogle Scholar
  13. Ekman P, Friesen WV (1978) Manual for the facial action coding system. Consulting Psychologists Press, Palo AltoGoogle Scholar
  14. Fusar-Poli P, Placentino A, Carletti F, Allen P, Landi P, Abbamonte M, Politi PL (2009) Laterality effect on emotional faces processing: ALE meta-analysis of evidence. Neurosci Lett 452(3):262–267.  https://doi.org/10.1016/j.neulet.2009.01.065 CrossRefPubMedGoogle Scholar
  15. Gainotti G (1972) Emotional behavior and hemispheric side of the lesion. Cortex 8(1):41–55.  https://doi.org/10.1016/S0010-9452(72)80026-1 CrossRefPubMedGoogle Scholar
  16. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184CrossRefGoogle Scholar
  17. Indersmitten T, Gur RC (2003) Emotion processing in chimeric faces: hemispheric asymmetries in expression and recognition of emotions. J Neurosci 23(9):3820–3825.  https://doi.org/10.1523/JNEUROSCI.23-09-03820.2003 CrossRefPubMedGoogle Scholar
  18. Levy J, Heller W, Banich MT, Burton LA (1983) Asymmetry of perception in free viewing of chimeric faces. Brain Cognit 2(4):404–419.  https://doi.org/10.1016/0278-2626(83)90021-0 CrossRefGoogle Scholar
  19. Marsili L, Agostino R, Bologna M, Belvisi D, Palma A, Fabbrini G, Berardelli A (2014) Bradykinesia of posed smiling and voluntary movement of the lower face in Parkinson’s disease. Parkinsonism Relat Disord 20(4):370–375.  https://doi.org/10.1016/j.parkreldis.2014.01.013 CrossRefPubMedGoogle Scholar
  20. Middleton FA, Strick PL (2000a) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31: 236–250.  https://doi.org/10.1016/S0165-0173(99)00040-5 CrossRefPubMedGoogle Scholar
  21. Middleton FA, Strick PL (2000b) Basal ganglia output and cognition: Evidence from anatomical, behavioral, and clinical studies. Brain Cognit.  https://doi.org/10.1006/brcg.1999.1099 CrossRefGoogle Scholar
  22. Moreno CR, Borod JC, Welkowitz J, Alpert M (1990) Lateralization for the expression and perception of facial emotion as a function of age. Neuropsychologia 28(2):199–209.  https://doi.org/10.1016/0028-3932(90)90101-S CrossRefPubMedGoogle Scholar
  23. Özekmekçi S, Benbir G, Özdogan FY, Ertan S, Kiziltan ME (2007) Hemihypomimia, a rare persistent sign in Parkinson’s disease: follow up of 11 patients. J Neurol 254(3):347–350.  https://doi.org/10.1007/s00415-006-0372-z CrossRefPubMedGoogle Scholar
  24. Ricciardi L, Bologna M, Morgante F, Ricciardi D, Morabito B, Volpe D, Fasano A (2015) Reduced facial expressiveness in Parkinson’s disease: a pure motor disorder? J Neurol Sci.  https://doi.org/10.1016/j.jns.2015.08.1516 CrossRefPubMedGoogle Scholar
  25. Ricciardi L, Visco-Comandini F, Erro R, Morgante F, Bologna M, Fasano A, Kilner J (2017) Facial emotion recognition and expression in Parkinson’s disease: an emotional mirror mechanism? PLoS One.  https://doi.org/10.1371/journal.pone.0169110 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Silberman EK, Weingartner H (1986) Hemispheric lateralization of functions related to emotion. Brain Cognit 5(3):322–353.  https://doi.org/10.1016/0278-2626(86)90035-7 CrossRefGoogle Scholar
  27. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653.  https://doi.org/10.1002/mds.23429 CrossRefPubMedGoogle Scholar
  28. Uitti RJ, Baba Y, Whaley NR, Wszolek ZK, Putzke JD (2005) Parkinson disease: handedness predicts asymmetry. Neurology 64(11):1925–1930.  https://doi.org/10.1212/01.WNL.0000163993.82388.C8 CrossRefPubMedGoogle Scholar
  29. Wager TD, Phan KL, Liberzon I, Taylor SF (2003) Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. NeuroImage 19(3):513–531.  https://doi.org/10.1016/S1053-8119(03)00078-8 CrossRefPubMedGoogle Scholar
  30. Young aW, Perrett DI, Calder aJ, Sprengelmeyer R, Ekman P (2002) Facial expressions of emotion: stimuli and tests (FEEST). Pslychoogy.  https://doi.org/10.1016/S0010-0277(97)00003-6 CrossRefGoogle Scholar
  31. Zingler VC, Strupp M, Jahn K, Brandt T (2005) Hemihypomimia in Parkinson’s disease. Eur Neurol 53(2):92–93.  https://doi.org/10.1159/000085505 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Lucia Ricciardi
    • 1
    Email author
  • Federica Visco-Comandini
    • 2
  • Roberto Erro
    • 3
  • Francesca Morgante
    • 1
    • 4
  • Daniele Volpe
    • 5
  • James Kilner
    • 2
  • Mark J. Edwards
    • 1
  • Matteo Bologna
    • 6
    • 7
    Email author
  1. 1.Neurosciences Research Centre, Molecular and Clinical Sciences InstituteSt George’s University of LondonLondonUK
  2. 2.Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of NeurologyUniversity College LondonLondonUK
  3. 3.Department of Medicine, Surgery and Dentistry, Center for Neurodegenerative Diseases (CEMAND)University of SalernoFiscianoItaly
  4. 4.Department of Clinical and Experimental MedicineUniversity of MessinaMessinaItaly
  5. 5.Neurorehabilitation DepartmentCasa di Cura “Villa Margherita”VicenzaItaly
  6. 6.Department of Human NeurosciencesSapienza University of RomeRomeItaly
  7. 7.IRCCS NeuromedPozzilliItaly

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