Research article
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40/35 35.2
± 6.5 [20; 50] 39.1
± 8 [24; 58] - (1 ,73) 5.49 0.02
Matrix [1; 19] 36/37
13.1 ± 2.4 [7; 18] 9.9 ± 2.5 [5; 15] - (1 ,71) 31.63 <0.001 Benton (/54) 39/38 46.9
± 3.5 [39; 52] 45 ± 3.2 [40; 53] - (1 ,75) 5.96 0.017 VOSP SDS (/20) -/38 -
± 0.6 [18; 20] - - - VOSP PD (/20) -/38 -
± 0.6 [18; 20] - - - VOSP NL (/10) -/38 -
± 0.9 [7; 10] - - - LARS [-15; 15] -/37 -
± 2.6 [-15; -7] - - - Disease duration (years) -/40 -
± 5.3 [1; 20] - - - Worst affected side (L/R) -/40 -
- - - LEDD (mg/day) -/40
- 1043.2
± 454.2 [250; 2355] - - - UPDRS III 1 (/108)
37/32 - 11.9 ± 8.9 [1; 33] 30.5
± 12.6 [14; 62.5] (1 ,67) 50.31 <0.001 Hoehn & Yahr 1 (/5)
38/39 - 1.2 ± 0.7 [0; 3] 2.1
± 1 [1; 5] (1 ,75) 23.43 <0.001 N = data available for each group: healthy participants/PD patients. 1 number of patients assessed during the ON and OFF DRT states: ON/OFF. VOSP SDS, PD and ND = Shape Detection Screening, Position Discrimination and Number Location subtests from the Visual and Object Space Perception battery (VOSP). df = degrees of freedom. For the participants who could not be assessed on the Matrix test, a minimum score of 130 on the Mattis Dementia Rating Scale [ 41 ] was nonetheless used to ascertain the absence of cognitive dysfunctions. doi:10.1371/journal.pone.0160329.t001 Fig 2. Decoding accuracy scores of the healthy controls and the PD patients whatever the emotion displayed (all) and as a function of emotion. Mean ± standard error and boxplot. doi:10.1371/journal.pone.0160329.g002 Facial Mimicry in Parkinson's Disease PLOS ONE | DOI:10.1371/journal.pone.0160329 July 28, 2016 6 / 20
Confounding emotions When the emotional nature of the error made was examined, analyses showed that the PD patients provided globally a similar pattern of confusion than the HC. However, quantitative and qualitative differences appeared for some aspects ( Fig 3 ). For angry avatars, the confound- ing emotion was mostly surprise, then fear and disgust, in both groups. For happy avatars, the confounding emotion was quasi-systematically surprise in both groups. For neutral avatars, the confounding emotion was sadness in both groups, then surprise among the PD patients. The group x non-target emotion interactions were statistically significant for happy ( χ² = 12.06, df = 5, p = 0.034) and neutral ( χ² = 25.21, df = 5, p<0.001) avatars but not for angry avatars ( χ² = 2.6, df = 5, p = 0.76). Surprise was more often selected by the PD patients than the HC for happy avatars ( χ² = 15.33, df = 1, p<0.001) and neutral avatars (χ² = 21.25, df = 1, p
did ( χ² = 17.06, df = 1, p<0.001). Facial reactions A statistically significant group x emotion x muscle x interval interaction effect was found ( χ² = 431.65, df = 76, p <0.001). In the HC, comparisons across emotions evidenced specific varia- tions in response to the emotion for each muscle ( Fig 4A ,
). From 400 ms after stimu- lus onset, corrugator activity decreased in response to expressions of joy whereas it increased in response to angry faces and showed an intermediate pattern in response to neutral expressions. Conversely, from 500 ms after stimulus onset, zygomaticus activity increased in response to expressions of joy whereas it remained quite stable or decreased slightly in response to angry or neutral avatars. The same applied to the orbicularis muscle from 700 ms after stimulus onset. Whatever the recording interval, the variations of these two muscles in response to angry ava- tars were not different from those observed in response to neutral expressions. In the PD patients, comparisons across emotions evidenced specific variations in response to the emotion Fig 3. Emotional nature of the misidentified expressions as a function of group and emotion displayed. Mean ± standard errors. Confusion percentage among the HC are shown in white; confusion percentage among the PD patients are shown in grey. doi:10.1371/journal.pone.0160329.g003 Facial Mimicry in Parkinson's Disease PLOS ONE | DOI:10.1371/journal.pone.0160329 July 28, 2016 7 / 20
for the corrugator muscle alone ( Fig 4A
, S3 Table
). From 700 ms after stimulus onset, corruga- tor activity decreased in response to expressions of joy, increased slightly in response to angry faces and showed an intermediate pattern in response to neutral expressions (there was no sig- nificant difference between neutral and angry avatars except from 1700 to 1900 ms). Among the PD patients, the responses of the zygomaticus and the orbicularis muscles did not vary across emotions whatever the interval. Comparisons between muscle responses confirmed these specific variations of muscular activity observed in response to emotions ( Fig 4B
; see S2 Appendix , S4 and S5 Tables).
The analyses also evidenced a statistically significant group x emotion x muscle interaction effect (
χ² = 1127.07, df = 4, p<0.001). Overall, the increased activity of the corrugator muscle in response to angry avatars was lower in the patients than in the HC ( χ² = 14.89, df = 1, p = 0.001). More precisely, corrugator activity in response to angry avatars differed between the groups from 1000 to 1200 ms and from 1900 to 2000 ms after stimulus onset ( Table 2
). Likewise, the overall increased activity in both the zygomaticus ( χ² = 78.96, df = 1, p<0.001) and the orbicularis ( χ² = 23.29, df = 1, p<0.001) muscles in response to happy avatars were greater in the HC than in the patients for whom these responses were almost non-existent. These significant inter-group differences appeared from 700 ms after stimulus onset for the zygomaticus muscle and from 900 ms for the orbicularis muscle ( Table 2 ). In addition, the overall decrease in corrugator activity in response to happy expressions tended to be lower in the patients compared to the HC ( χ² = 6.65, df = 1, p = 0.089). Regarding the mean EMG amplitudes measured at baseline, analysis showed a statistically significant group effect ( χ² = 5.49, df = 1, p = 0.019) as well as a statistically significant group x muscle interaction effect ( χ² = 124.78, df = 2, p<0.001). The mean EMG amplitudes measured at baseline were higher among the PD patients compared to the HC (mean ± standard error: PD patients = 5.25 ± 0.08 μV; HC = 3.91 ± 0.05 μV) but this effect was carried by the zygomati- cus activity (PD = 6.02 ± 0.18 vs. HC = 3.69 ± 0.1 μV; χ² = 16.38, df = 1, p<0.001) as no statistically significant group difference emerged for the corrugator and orbicularis activities Fig 4. EMG responses (relative to baseline) recorded on sequential 100 ms intervals of stimulus exposure according to muscle, group and emotion factors. Mean ± standard error. (A) emotion-specific variations for each recorded muscle; (B) muscle-specific variations in response to the emotion displayed. doi:10.1371/journal.pone.0160329.g004 Facial Mimicry in Parkinson's Disease PLOS ONE | DOI:10.1371/journal.pone.0160329 July 28, 2016 8 / 20
(corrugator: PD = 5.19 ± 0.1 vs. HC = 4.49 ± 0.09 μV; χ² = 1.16, df = 1, p = 0.85 and orbicularis: PD = 4.56 ± 0.12 vs. HC = 3.54 ± 0.05 μV; χ² = 3.65, df = 1, p = 0.17). Finally, none of the clinical characteristics of the patients (disease duration, worst affected side, LEDD, Hoehn and Yahr stages and UPDRS III scores ON and OFF DRT) had a statistically significant effect on muscle responses whatever the emotion or the period of stimulus exposure at the adjusted significance threshold for multiple comparisons (3 muscles x 3 emotions x 4 peri- ods, adjusted α value = 0.001). The effects obtained at the significant threshold of 0.05 are none- theless shown in S3 Appendix . Facial reactions and emotion decoding accuracy At the adjusted significance threshold for multiple comparisons (3 emotions x 4 periods, adjusted
α value = 0.004), only corrugator responses had a statistically (or quasi-) significant effect on decoding accuracy of expressions of joy: in both groups, for all the 500 ms recording periods except the first, the probability of accurately identifying joy increased with the corruga- tor relaxation (500 –1000: χ² = 8.14, df = 1, p = 0.004; 1000–1500: χ² = 9.21, df = 1, p = 0.002 and 1500
–2000: χ² = 7.5, df = 1, p = 0.006). At this threshold, we still noted a statistically mar- ginal group x zygomaticus muscle responses interaction in the joy condition in the first 500 ms period ( χ² = 5.84, df = 1, p = 0.016): unlike what was observed in the patients, the probability of Table 2. Inter-groups comparisons of EMG responses recorded on sequential 100 ms intervals of stimulus exposure. Interval CORRU
—Angry ZYGO
—Happy ORBI
—Happy 0 –100 (0.3) ns (0.2) ns
(0.2) ns 100
–200 (1.5) ns
(0.1) ns (0.3) ns
200 –300
(0.03) ns (0.3) ns
(0.4) ns 300
–400 (0.08) ns (0.2) ns (0.1) ns
400 –500
(2) ns (1.3) ns
(0.1) ns 500
–600 (4.4) ns
(4.5) ns (1.2) ns
600 –700
(7) ns (13.15) = 0.052 (3.6) ns 700
–800 (6.2) ns
(28.7) <0.001 (6.4) ns
800 –900
(5.6) ns (50.7)
<0.001 (10.3) ns 900 –1000
(7.4) ns (73.2)
<0.001 (15.6)
<0.05 1000
–1100 (14)
<0.05 (97.3)
<0.001 (19.9)
<0.005 1100
–1200 (14.5)
<0.05 (107.1)
<0.001 (22.5)
<0.001 1200
–1300 (11.4) ns (97)
(28.7)
<0.001 1300
–1400 (12.4) = 0.079 (95.9)
(34.2)
<0.001 1400
–1500 (7.8) ns
(94.3) <0.001 (37.1)
<0.001 1500
–1600 (9.7) ns
(93.7) <0.001 (34)
<0.001 1600
–1700 (10.3) ns (73.1)
(21.8)
<0.005 1700
–1800 (11.7) ns (51.5)
(13.9)
<0.05 1800
–1900 (10.8) ns (53.6)
(17.3)
<0.01 1900
–2000 (19.8)
<0.005 (56.1)
<0.001 (25.8)
<0.001 Only the inter-groups comparisons of EMG responses recorded for the corrugator muscle in response to angry avatars (CORRU —Angry), the zygomaticus in response to happy avatars (ZYGO—Happy) and the orbicularis in response to happy avatars (ORBI —Happy) are shown here. No other comparisons were signi ficant (all p>0.1). Test statistics (χ 2 ) are shown in brackets. Figures in bold denote statistically signi ficant differences (p value <0.05). ns = non statistically significant = p value>0.1 doi:10.1371/journal.pone.0160329.t002 Facial Mimicry in Parkinson's Disease PLOS ONE | DOI:10.1371/journal.pone.0160329 July 28, 2016 9 / 20
accurately identifying joy appeared to increase with the contractions of the zygomaticus muscle in the first 500 ms of stimulus exposure in the HC. The effects associated with a significance threshold of 0.05 are nonetheless shown in S4 Appendix . Discussion The current study was designed to evaluate the role of facial mimicry in recognition of facial emotion. For this purpose, we investigated for the first time EMG responses to facial expres- sions among patients suffering from Parkinson ’s disease (PD) in a facial emotion recognition paradigm. Three main results emerged from our analyses. Firstly, in accordance with the litera- ture, the PD patients were less accurate in decoding facial expressions of joy and neutral faces compared to the healthy controls (HC). Secondly, the facial expressions were mimicked as expected. However, the emotion-specific EMG variations were disturbed in the PD patients with weaker than normal corrugator reactions in response to angry faces and with almost no reactions from the orbicularis and the zygomaticus muscles in response to happy avatars. Thirdly, the analyses highlighted statistically significant effects of the facial reactions on emo- tion decoding accuracy. Notably, the corrugator relaxation as well as the zygomatic contraction in response to happy faces is correlated to the decoding of joy. Many studies have demonstrated the negative impact of PD in the recognition of emotion expressed on faces [ 42 – 50 ] but other studies have failed to confirm these observations [ 51 –
]. The review by Assogna and collaborators [ 19 ] and the meta-analysis by Gray and Tickle-Deg- nen [ 20 ] identified different factors to explain this discrepancy: the implementation of small samples, inadequate control for demographic characteristics of the participants, the depression status, the presence of cognitive or visuospatial deficits and the influence of dopamine replace- ment therapy (DRT). In this study, we used large samples (n = 40 in both groups). We excluded individuals suffering from depression, apathy, cognitive and visuospatial deficits or impair- ments in facial processing. We also took into account the sociodemographic and neuropsycho- logical characteristics of the participants in the statistical analyses. None of these potential confounding factors had a statistically significant effect except for age. As age had the same negative effect in the two groups and since this effect is reported in the literature [ 55 ], we did not give further consideration to this point. Finally, we examined the effect of DRT and other clinical features of the patients on emotion decoding accuracy. Our results confirmed the negative impact of PD in emotion recognition for happy and neu- tral faces. Conversely, the PD patients did not differ from the HC in the recognition of anger. Furthermore, the nature of the misidentified expressions was globally similar between the groups. Only quantitative and qualitative differences emerged regarding the recognition of joy and neutral expressions. Whatever the emotion displayed, surprise was the most frequent con- founding emotion especially among the PD patients. Then, both the HC and the PD patients confounded anger with other negative emotions and neutral with sadness. When the partici- pants had to recognize joy expressions, surprise was the only source of confusion. Since one can be positively surprised, negatively surprised and even neither positively nor negatively sur- prised but just astonished, surprise is ambiguous. This confounding emotion highlighted diffi- culties to recognize emotions among PD patients. This effect is supported by studies which depicted surprise as a source of confusion and showed a specific deficit of surprise recognition among PD patients [ 23 , 45 ]. Likewise, the similar nature of the misidentified expressions between HC and PD patients depicted a normal but a noised process of facial emotions. These findings fit with the presumed role of the basal ganglia-thalamocortical connections underlying emotional processing described by Péron and collaborators [ 56 ]. According to the model pro- posed by these authors, a dysfunction in the pathways involving the basal ganglia as it ’s Facial Mimicry in Parkinson's Disease PLOS ONE | DOI:10.1371/journal.pone.0160329 July 28, 2016 10 / 20
observed in PD could prevent correctly inhibiting the non relevant information and/or cor- rectly activating the relevant information causing the emotional judgements to be disturbed. The fact that the patients ’ abilities to recognize emotions tended to increased with the LEDD is fully consistent with the purported role of dopamine in the perception of emotion [ 57 ]. A relationship between DRT and emotion recognition is in accordance with both the amygdala dysfunction hypothesis and the dopamine depletion hypothesis in PD. Experimental data support these explanations: for example, the restoration of amygdala response in PD patients perceiving facial emotions during a dopamine-replete state compare to an hypodopa- minergic state [ 58 ] and the better performances in recognizing facial emotions in medicated compared to unmedicated PD patients [ 50 ]. The absence of a negative impact of PD in the recognition of anger fits the idea of Lawrence and collaborators [ 48 ,
] that DRT could mask any deficit present in PD especially for anger recognition. In 2007, these authors assessed performances of emotion recognition in PD patients withdrawn from dopamine replacement therapy and showed indeed an anger-specific deficit of recognition among these patients with a spared recognition of other facial emotions (disgust, fear, sadness, joy and surprise). Likewise, Dujardin and collaborators [ 45 ] highlighted a deficit in anger recognition in PD patients who had not yet received any medication. Besides, from a methodological point of view, our study had some characteristics which may play a role in our results. First, we used dynamic expressions in order to provide more ecological stimuli. Considering the importance of dynamic features of the stimuli in the emotion recognition pro- cess, the used of static faces could artificially cause a deficit in emotion recognition in PD, or at least widened it [ 19 ,
]. Like us, Kan and collaborators [ 47 ] did not highlighted a deficit con- cerning the recognition of anger when exposing participants to dynamic facial expressions and they showed that the performances of the patients were largely lower when they had to recog- nize sadness, disgust and anger from static stimuli compared to dynamic expressions. At last, another argument to explain this absence of group difference concerning the recognition of anger could also reside in the clinical characteristics of the patients. Indeed, the patients involved in the current study did not present any potential non-motor symptoms (cognitive and visuo-perceptual impairment, face processing deficit, depression or apathy) which could have interfered with the performances on the affective recognition test [ 19 ,
]. To explain the deficit of facial emotion recognition in PD, some authors have suggested functional and/or anatomical dysfunctions in brain structures such as the amygdala, the basal ganglia including the ventral striatum, the orbito-frontal cortex and the insula as well as the impairment of dopamine transmission in the mesocorticolimbic pathway [ 18 – 20 ]. However, other authors have argued that PD patients could experience deficits in recognizing emotion because of a reduced ability to mimic the perceived emotion. In fact, the presence of a common neural substrate —as part of the mirror neurons system—underlying the ability to express emo- tions and to recognize facial emotions expressed by others, suggests that facial amimia could contribute to the deficit in recognition of emotion in PD [ 21 ,
]. With regard to the EMG responses, our methodology enabled us to evidence emotion-spe- cific facial reactions 500 ms after stimulus onset as described in the literature: among the HC, facial reactions to angry expressions were characterized by an increased activity of the corruga- tor muscle —an important muscle for frowning in expressions like anger or sadness—and a slight relaxation of the zygomaticus and the orbicularis —muscles involved in the production of smiling expressions by raising the corners of the mouth and forming “crow’s feet” on the outer corners of a person ’s eyes [ 62 ]
pattern. These variations, which occurred only from the first 500 ms after stimulus onset, have been widely highlighted in previous studies and are considered to reflect facial mimicry Yüklə 0,9 Mb. Dostları ilə paylaş:
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