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.
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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
References
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
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
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
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
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
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
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
Cattaneo L, Pavesi G (2014) The facial motor system. Neurosci Biobehav Rev. https://doi.org/10.1016/j.neubiorev.2013.11.002
Crosiers D, MaréChal E, van Ael Y, Cras P (2011) Left-sided hemihypomimia in Parkinson’s disease. Acta Neurologica Belgica 111(3):225–227
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
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
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
Ekman P, Friesen WV (1978) Manual for the facial action coding system. Consulting Psychologists Press, Palo Alto
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
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
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 55:181–184
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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Ricciardi, L., Visco-Comandini, F., Erro, R. et al. Emotional facedness in Parkinson’s disease. J Neural Transm 125, 1819–1827 (2018). https://doi.org/10.1007/s00702-018-1945-6
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DOI: https://doi.org/10.1007/s00702-018-1945-6