On the analysis of EEG power, frequency and asymmetry in Parkinson’s disease during emotion processing

Behavioral and Brain Functions

Marimuthu Satiyan¹  Edgar Mesquita³  Ramaswamy Palaniappan²  Khairiyah Mohamad⁴  Kenneth Sundaraj¹  Mohd Iqbal Omar¹  Norlinah Mohamed Ibrahim⁴  Murugappan Murugappan¹  Rajamanickam Yuvaraj¹ 

[1]School of Mechatronic Engineering, Universiti Malaysia Perlis (UniMAP), Arau, Malaysia

[2]Faculty of Science and Engineering, University of Wolverhampton, Telford, UK

[3]University of Minho, Braga, Portugal

[4]Neurology Unit, Department of Medicine, UKM Medical Center, Kuala Lumpur, Malaysia

关键词: Hemispheric asymmetry;    Frequency bands;    EEG Power;    Emotion;   

Others  :  791856
DOI  :  10.1186/1744-9081-10-12

 received in 2013-11-04, accepted in 2014-03-10,  发布年份 2014

【 摘 要 】

Objective

While Parkinson’s disease (PD) has traditionally been described as a movement disorder, there is growing evidence of disruption in emotion information processing associated with the disease. The aim of this study was to investigate whether there are specific electroencephalographic (EEG) characteristics that discriminate PD patients and normal controls during emotion information processing.

Method

EEG recordings from 14 scalp sites were collected from 20 PD patients and 30 age-matched normal controls. Multimodal (audio-visual) stimuli were presented to evoke specific targeted emotional states such as happiness, sadness, fear, anger, surprise and disgust. Absolute and relative power, frequency and asymmetry measures derived from spectrally analyzed EEGs were subjected to repeated ANOVA measures for group comparisons as well as to discriminate function analysis to examine their utility as classification indices. In addition, subjective ratings were obtained for the used emotional stimuli.

Results

Behaviorally, PD patients showed no impairments in emotion recognition as measured by subjective ratings. Compared with normal controls, PD patients evidenced smaller overall relative delta, theta, alpha and beta power, and at bilateral anterior regions smaller absolute theta, alpha, and beta power and higher mean total spectrum frequency across different emotional states. Inter-hemispheric theta, alpha, and beta power asymmetry index differences were noted, with controls exhibiting greater right than left hemisphere activation. Whereas intra-hemispheric alpha power asymmetry reduction was exhibited in patients bilaterally at all regions. Discriminant analysis correctly classified 95.0% of the patients and controls during emotional stimuli.

Conclusion

These distributed spectral powers in different frequency bands might provide meaningful information about emotional processing in PD patients.

【 授权许可】

   
2014 Yuvaraj et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

Figure 10.

Figure 11.

Figure 12.

Figure 13.

Figure 14.

【 参考文献 】

• [1]Valls-Sole J, Valldeoriola F: Neurophysiological correlate of clinical signs in Parkinson’s disease. Clin Neurophysiol 2002, 113:792-805.
• [2]Betarbet R, Sherer TB, Greenamyre JT: Animal models of Parkinson’s disease. Bioessays 2002, 24:308-318.
• [3]Chen HL, Huang CC, Yu XG, Xu X, Sun X, Wang G, Wang SJ: An efficient diagnosis system for detection of Parkinson’s disease using fuzzy k-nearest neighbor approach. Expert Syst Appl 2013, 40:263-271.
• [4]Savitt JM, Dawson VL, Dawson TM: Diagnosis and treatment of Parkinson disease: molecules to medicine. J Clin Invest 2006, 116:1744-1754.
• [5]Dujardin K, Blairy S, Defebvre L, Duhem S, Noël Y, Hess U, Destée A: Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia 2004, 42:239-250.
• [6]Janvin C, Aarsland D, Larsen JP, Hugdahl K: Neuropsychological profile of patients with Parkinson’s disease without dementia. Dement Geriatr Cogn Disord 2003, 15:126-131.
• [7]Park A, Stacy M: Non-motor symptoms in Parkinson’s disease. J Neurol 2009, 256(Suppl.3):S293-S298.
• [8]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.
• [9]Lawrence AD, Goerendt IK, Brooks DJ: Impaired recognition of facial expression of anger in Parkinson’s disease patients acutely withdrawn from dopamine replacement therapy. Neuropsychologia 2007, 45:65-74.
• [10]Sprengelmeyer R, Young AW, Mahn K, Schroeder U, Woitalla D, Büttner T, Kuhn W, Przuntek H: Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia 2003, 41:1047-1057.
• [11]Dara C, Monetta L, Pell MD: Vocal emotion processing in Parkinson’s disease: Reduced sensitivity to negative emotions. Brain Res 2008, 1188:100-111.
• [12]Paulmann S, Pell MD: Dynamic emotion processing in Parkinson’s disease as a function of channel availability. J Clin Exp Neuropsychol 2010 Oct; 32(8):822–35 2010, 32:822-835.
• [13]Bowers D, Miller K, Mikos A, Kirsch-Darrow L, Springer U, Fernandez H, Foote K, Okun M: Startling facts about emotion in Parkinson’s disease: blunted reactivity to aversive stimuli. Brain 2006, 129:3356-3365.
• [14]Miller KM, Okun MS, Marsiske M, Fennell EB, Bowers D: Startle reflex hyporeactivity in Parkinson’s disease: an emotion-specific or arousal-modulated deficit? Neuropsychologia 2009, 47:1917-1927.
• [15]Schröder C, Mobes J, Schutze M, Szymanowski F, Nager W, Bangert M, Munte TF, Dengler R: Perception of emotional speech in Parkinson’s disease. Mov Disord 2006, 21:1774-1778.
• [16]Wieser MJ, Klupp E, Weyers P, Pauli P, Weise D, Zeller D, Classen J, Muhlberger A: Reduced early visual emotion discrimination as an index of diminished emotion processing in Parkinson’s disease? - Evidence from event-related brain potentials. Cortex 2012, 48:1207-1217.
• [17]Adolphs R, Schul R, Tranel D: Intact recognition of facial emotion in Parkinson’s disease. Neuropsychology 1998, 12:253-258.
• [18]Caekebeke JF, Jennekens-Schinkel A, VanderLinden ME, Buruma OJ, Roos RA: The interpretation of dysprosody in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 1991, 54:145-148.
• [19]Garrido-Vásquez P, Pell MD, Paulmann S, Strecker K, Schwarz J, Kotz SA: An ERP study of vocal emotion processing in asymmetric Parkinson’s disease. Soc Cogn Affect Neurosci 2013, 8(8):918-927.
• [20]Madeley P, Ellis A, Mindham R: Facial expressions and Parkinson’s disease. Behav Neurol 1995, 8:115-119.
• [21]Pell MD, Leonard CL: Facial expression decoding in early Parkinson’s disease. Cogn Brain Res 2005, 23:327-340.
• [22]Suzuki A, Hoshino T, Shigemasu K, Kawamura M: Disgust-specific impairment of facial expression recognition in Parkinson’s disease. Brain 2006, 129:707-717.
• [23]Ariatti A, Benuzzi F, Nichelli P: Recognition of emotions from visual and prosodic cues in Parkinson’s disease. Neurol Sci 2008, 29:219-227.
• [24]Yip JT, Lee TM, Ho SL, Tsang KL, Li LS: Emotion recognition in patients with idiopathic Parkinson’s disease. Mov Disord 2003, 18:1115-1122.
• [25]Ventura MI, Baynes K, Sigvardt KA, Unruh AM, Acklin S, Kirsch HE, Disbrow EA: Hemispheric asymmetries and prosodic emotion recognition deficits in Parkinson’s disease. Neuropsychologia 2012, 50:1936-1945.
• [26]Bechara A, Damasio H, Damasio AR: Emotion, decision making and the orbifrontal cortex. Cereb Cortex 2000, 10:295-307.
• [27]Schmidt LA, Trainor LJ: Frontal brain electrical activity (EEG) distinguishes valence and intensity of musical emotions. Cogn Emo 2001, 15:487-500.
• [28]Sarlo M, Buodo G, Poli S, Palomba D: Changes in EEG alpha power to different disgust elicitors: the specificity of mutilations. Neurosci Lett 2005, 382:291-296.
• [29]Aftanas LI, Reva NV, Varlamov AA, Pavlov SV, Makhnev VP: Analysis of evoked EEG synchronization and desynchronization in emotional activation in humans: temporal and topographic characteristics. Neurosci Behav Physiol 2004, 34:859-867.
• [30]Sammler D, Grigutsch M, Fritz T, Koelsch S: Music and emotion: electrophysiological correlates of the processing of pleasant and unpleasant music. Psychophysiology 2007, 44:293-304.
• [31]Schutter DJL, Putman P, Hermans E, van Honk J: Parietal electroencephalogram beta asymmetry and selective attention to angry facial expressions in healthy human subjects. Neurosci Lett 2001, 314:13-16.
• [32]Balconi M, Lucchiari C: Consciousness and arousal effects on emotional face processing as revealed by brain oscillations. A gamma band analysis. Int J Psychophysiol 2008, 67:41-46.
• [33]Hoehn MM, Yahr MD: Parkinsonism: Onset, Progression and mortality. Neurology 1967, 17:427-442.
• [34]Fahn S, Elton RL, Committee M: Unified Parkinson’s disease rating scale. In: Fahn’s, Marsden CD, Calne DB, Goldstein M, Clane DB Recent Developments in Parkinson’s Disease Macmillan Health Care Information; Florham Park 1987, 2:153-163.
• [35]Folstein MF, Folstein SE, Mchugh PR: Mini-mental state examination: a practical method for grading the cognitive state of patients. Psychol Res 1975, 12:189-198.
• [36]Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J: An inventory for measuring depression. Arch Gen Psychiatry 1961, 4:561-571.
• [37]Oldfield RC: The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 1971, 9:97-113.
• [38]Kim J, Andre E: Emotion recognition based on physiological changes in music listening. IEEE Trans Pattern Anal Mach Intell 2008, 30:2067-2083.
• [39]Ekman P, Friesen WV: Universals and cultural differences in the judgments of facial expressions of emotion. J Pers Soc Psychol 1987, 53:712-714.
• [40]Lang PJ: The emotion probe: studies of motivation and attention. Am Psychol 1995, 50:372-385.
• [41]Gray HM, Tickle-Degnen L: A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology 2010, 24:176-191.
• [42]Péron J, Dondaine T, Jeune FL, Grandjean D, Vérin M: Emotional processing in Parkinson’s disease: a systematic review. Mov Disord 2012, 27:186-199.
• [43]Baumgartner T, Esslen M, Jancke L: From emotion perception to emotion experience: Emotions evoked by pictures and classical music. Int J Psychophysiol 2006, 60:34-43.
• [44]Davidson RJ: Anterior cerebral asymmetry and the nature of emotion. Brain Cogn 1992, 20:125-151.
• [45]Gross JJ, Levenson RW: Emotion elicitation using films. Cogn Emotion 1995, 9:87-108.
• [46]Murugappan M, Rizon M, Nagarajan R, Yaacob S: An investigation on visual and audiovisual stimulus based human emotion recognition using EEG. Int J Med Eng Informat 2009, 1:342-356.
• [47]Petrantonakis PC, Hadjileontiadis LJ: A novel emotion elicitation index using frontal brain asymmetry for enhanced EEG-based emotion. IEEE Trans Inf Technol Biomed 2011, 15:737-746.
• [48]Kim KH, Bang SW, Kim SR: Emotion recognition system using short-term monitoring of physiological signal. Med Biol Eng Comput 2004, 42:419-427.
• [49]Wang Y, Guan L: Recognizing human emotional state from audiovisual signals. IEEE Trans Multimed 2008, 10:659-668.
• [50]Lang PJ, Greenwald MK, Bradley MM, Hamm AO: Looking at the pictures: affective, facial, visceral, and behavioral reactions. Psychophysiology 1993, 30:261-273.
• [51]Bradley MM, Lang PJ: International affective digitized sounds (2nd Edition; IADS-2): Affective ratings of sounds and instruction manual. Gainesville, FL: Technical Report B-3 University of Florida; 2007.
• [52]Jerritta S, Murugappan M, Wan K, Yaacob S: Classification of emotional states from electrocardiogram signals: a non-linear approach based on hurst. Biomed Eng Online 2013, 12:44-62. BioMed Central Full Text
• [53]Brown L, Grundlehner B, Penders J: Towards wireless emotional valence detection from EEG. In Proceedings of the IEEE Engineering in Medicine and Biology Society. IEEE Eng Med Biol Soc.; 2011:2188-2191.
• [54]Mikels J, Fredrickson B, Larkin G, Lindberg C, Maglio S, Reuter-Lorenz P: Emotional Category data on images from the international affective picture system. Behav Res Methods 2005, 37:630-636.
• [55]Redondo J, Fraga I, Padron I, Pineiro A: Affective ratings of sound stimuli. Behav Res Methods 2008, 40:784-790.
• [56]Kim J: Bimodal emotion recognition using speech and physiological changes. In Robust Speech Recognition and Understanding. Edited by Grimm M, Kroschel K. Vienna, Austria: I-Tech Education and Publishing; 2007:265-280.
• [57]Hamdi H, Richard P, Suteau A, Allain P: Emotion Assessment for Affective Computing Based on Physiological Responses. In Conference Proceedings Fuzzy Systems (FUZZ-IEEE), IEEE International Conference on, World Congress on Computational Intelligence (WCCI). Brisbane, QLD: FUZZ-IEEE; 2012:1-8.
• [58]Petrantonakis PC, Hadjileontiadis LJ: Emotion recognition from brain signals using hybrid adaptive filtering and higher order crossings analysis. IEEE Trans Affect Comput 2010, 1:81-96.
• [59]Gotlib IH, Raganathan C, Rosenfeld JP: Frontal EEG alpha asymmetry, depression, and cognitive functioning. Cogn Emo 1998, 12:449-478.
• [60]Chotas HG, Bourne JR, Teschan PE: Heuristic techniques in the quantification of the electroencephalogram in renal failure. Comput Biomed Res 1979, 12:299-312.
• [61]John ER, Prichep L, Easton P: Neurometrics: computer assisted differential diagnosis of brain dysfunctions. Science 1988, 239:162-169.
• [62]Prichep L, John E: QEEG profiles of psychiatric disorders. Brain Topogr 1992, 4:249-257.
• [63]Gasser T, Bacher P, Mocks J: Transformations towards the normal distribution of broad spectral parameters of the EEG. Electroencephalogr Clin Neurophysiol 1982, 53:119-124.
• [64]Knott V, Mahoney C, Kennedy S, Evans K: EEG power, frequency, asymmetry, and coherence in male depression. Psychiatry Res 2001, 106:123-140.
• [65]Marosi E, Rodríguez H, Yanez G, Bernal J, Rodríguez M, Fernández T, Silva J, Reyes A, Guerrero V: Broad band spectral measurements of EEG during emotional tasks. Int J Neurosci 2001, 104:251-279.
• [66]John ER, Prichep L, Easton P: Normative data banks and neurometrics: basic concepts, methods and results of norm constructions. In Methods of Analysis of Brain Electric and Magnetic Signals Handbook of Electroencephalography and Clinical Neurophysiology, Revised Series. Edited by Gevins A, Remond A. Amsterdam: 1 Elsevier; 1987:449-495.
• [67]Jennings J, Wood C: The adjustment procedure for repeated measures analysis of variance. Psychophysiology 1976, 13:277-278.
• [68]Cohen H, Gagne MH, Hess U, Pourcher E: Emotion and object processing in Parkinson’s disease. Brain Cogn 2010, 72:457-463.
• [69]Neufeld MY, Inzelberg R, Korczyn AD: EEG in demented and non-demented parkinsonian patients. Acta Neurol Scand 1988, 78:1-5.
• [70]Yeager CL, Alberts WW, Denature LD: Effect of stereotaxic surgery upon electroencephalographic status of parkinsonian patients. Neurology 1966, 16:904-910.
• [71]Morita A, Kamei S, Serizawa K, Mizutani T: The relationship between slowing EEGs and the progression of Parkinson’s disease. J Clin Neuropsychol 2009, 26:426-429.
• [72]Barns NMP, Rickards H, Cavanna AE: The prevalence and clinical characteristics of pathological gambling in Parkinson’s disease: an evidence-based review. Funct Neurol 2010, 25:9-13.
• [73]Spencer AH, Rickards H, Fasano A, Cavanna AE: The prevalence and clinical characteristics of punding in Parkinson’s disease. Mov Disord 2011, 26:578-586.
• [74]Balarajah S, Cavanna AE: The pathophysiology of impulse control disorders in Parkinson disease. Behav Neurol 2013, 26:237-244.
• [75]Yuvaraj R, Murugappan M, Norlinah MI, Sundaraj K, Khairiyah M: Review of emotion recognition in stroke patients. Dement Geriatr Cogn Disord 2013, 36:179-196.
• [76]Adolphs R, Damasio H, Tranel D, Damasio AR: Corticle systems for the recognition of emotion in facial expressions. J Neurosci 1996, 16:7678-7687.
• [77]Davidson R, Irvin W: The functional neuroanatomy of emotion and affective style. Trends Cogn Sci 1999, 3:11-21.
• [78]Tessitore A, Hariri A, Fera F, Smith W, Chase T, Hyde T, Weinberger D, Mattay V: Dopamine modulates the response of the human amygdala: A Study in Parkinson’s disease. J Neurosci 2002, 22:9099-9103.
• [79]Yoshimura N, Kawamura M, Masaoka Y, Homma I: The amygdala of patients with Parkinson’s disease is silent in response to fearful facial expressions. Neuroscience 2005, 131:523-534.
• [80]Cancelliere AEB, Kertesz A: Lesion localization in acquired deficits of emotional expression and comprehension. Brain Cogn 1990, 13:133-147.
• [81]Salgado-Pineda P, Delaveau P, Blin O, Nieoullon A: Dopaminergic contribution to the regulation of emotional perception. Clin Neuropharmacol 2005, 28:228-237.
• [82]Lawrence AD, Calder AJ, McGowan SW, Grasby PM: Selective disruption of the recognition of facial expressions of anger. Neuroreport 2002, 13:881-884.
• [83]Lotze M, Reimold M, Heymans U, Laihinen A, Patt M, Halsband U: Reduced ventrolateral fMRI response during observation of emotional gestures related to the degree of dopaminergic impairment in Parkinson disease. J Cogn Neurosci 2009, 21:1321-1331.
• [84]Takahashi H, Yahata N, Koeda M, Takano A, Asai K, Suhara T, Okubof Y: Effects of dopaminergic and serotonergic manipulation on emotional processing: A pharmacological fMRI study. Neuroimage 2005, 27:991-1001.
• [85]Delaveau P, Salgado-Pineda P, Wicker B, Micallef-Roll J, Blin O: Effect of levodopa on healthy volunteers’ facial emotion perception: an FMRI study. Clin Neuropharmacol 2005, 28:255-261.