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Inter-hemispheric EEG coherence analysis in Parkinson’s disease: Assessing brain activity during emotion processing

  • Neurology and Preclinical Neurological Studies - Original Article
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Abstract

Parkinson’s disease (PD) is not only characterized by its prominent motor symptoms but also associated with disturbances in cognitive and emotional functioning. The objective of the present study was to investigate the influence of emotion processing on inter-hemispheric electroencephalography (EEG) coherence in PD. Multimodal emotional stimuli (happiness, sadness, fear, anger, surprise, and disgust) were presented to 20 PD patients and 30 age-, education level-, and gender-matched healthy controls (HC) while EEG was recorded. Inter-hemispheric coherence was computed from seven homologous EEG electrode pairs (AF3–AF4, F7–F8, F3–F4, FC5–FC6, T7–T8, P7–P8, and O1–O2) for delta, theta, alpha, beta, and gamma frequency bands. In addition, subjective ratings were obtained for a representative of emotional stimuli. Interhemispherically, PD patients showed significantly lower coherence in theta, alpha, beta, and gamma frequency bands than HC during emotion processing. No significant changes were found in the delta frequency band coherence. We also found that PD patients were more impaired in recognizing negative emotions (sadness, fear, anger, and disgust) than relatively positive emotions (happiness and surprise). Behaviorally, PD patients did not show impairment in emotion recognition as measured by subjective ratings. These findings suggest that PD patients may have an impairment of inter-hemispheric functional connectivity (i.e., a decline in cortical connectivity) during emotion processing. This study may increase the awareness of EEG emotional response studies in clinical practice to uncover potential neurophysiologic abnormalities.

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Notes

  1. The following pictures were used for emotion induction: Disgust 1945, 2352.2, 3000, 3010, 3015, 3030, 3051, 3060, 3061, 3071, 3080, 3110, 3120, 3130, 3140, 3150, 3160, 3250, 3400, 7360, 7361, 7380, 8230, 9040, 9042, 9181, 9290, 9300, 9320, 9330, 9373, 9390, 9405, 9490, 9570, 9830; Fear 1019, 1022, 1030, 1040, 1050, 1051, 1052, 1070, 1080, 1090, 1110, 1111, 1113, 1120, 1200, 1201, 1220, 1230, 1240, 1280, 1274, 1300, 1301, 1302, 1321, 1390, 1930, 1931, 3280, 5970, 5971, 5972, 6370, 9584, 9594, 9592; Sadness 2205, 2271, 2276, 2490, 2520, 2590, 2700, 2800, 2900, 3220, 3230, 3300, 3301, 3350, 6570, 6838, 8010, 9000, 9041, 9050, 9120, 9190, 9210, 9220, 9331, 9410, 9415, 9470, 9520, 9530, 9561, 9611, 9910, 9911, 9920, 9921.

  2. The following sounds were used for emotion induction: Disgust 134, 115, 251, 262, 284, 698, 702, 711, 712, 713, 714, 720, 728, 729, 730, 732, 812, 813; Fear 106, 133, 170, 171, 275, 276, 277, 279, 291, 312, 378, 380, 424, 425, 500, 626, 627, 699, 817; Sadness 115, 150, 260, 261, 278, 280, 285, 286,290, 293, 295, 310, 311, 368, 403, 420, 422, 501, 600, 625.

References

  • Adolphs R, Damasio H, Tranel D, Damasio AR (1996) Cortical systems for the recognition of emotion in facial expressions. J Neurosci 16:7678–7687

    CAS  PubMed  Google Scholar 

  • Adolphs R, Schul R, Tranel D (1998) Intact recognition of facial emotion in Parkinson’s disease. Neuropsychology 12(2):253–258

    Article  CAS  PubMed  Google Scholar 

  • Ariatti A, Benuzzi F, Nichelli P (2008) Recognition of emotions from visual and prosodic cues in Parkinson’s disease. Neurol Sci 29(4):219–227

    Article  PubMed  Google Scholar 

  • Bastiaanse R, Leenders KL (2009) Language and Parkinson’s disease. Cortex 45(8):912–914

    Article  PubMed  Google Scholar 

  • Baumgartner T, Esslen M, Jancke L (2006) From emotion perception to emotion experience: emotions evoked by pictures and classical music. Int J Psychophysiol 60(1):34–43

    Article  PubMed  Google Scholar 

  • Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571

    Article  CAS  PubMed  Google Scholar 

  • Beyer MK, Janvin CC, Larsen JP, Aarsland D (2007) A magnetic resonance imaging study of patients with Parkinson’s disease with mild cognitive impairment and dementia using voxel-based morphometry. J Neurol Neurosurg Psychiatry 78(3):254–259

    Article  PubMed Central  PubMed  Google Scholar 

  • Blair RJR, Morris JS, Frith CD, Perrett DI, Dolan RJ (1999) Dissociable neural responses to facial expressions of sadness and anger. Brain 122:883–893

    Article  PubMed  Google Scholar 

  • Bouchard TP, Malykhin N, Martin WR, Hanstock CC, Emery DJ, Fisher NJ, Camicioli RM (2008) Age and dementia-associated atrophy predominates in the hippocampal head and amygdala in Parkinson’s disease. Neurobiol Aging 29(7):1027–1039

    Article  PubMed  Google Scholar 

  • Bowers D, Miller K, Mikos A, Kirsch-Darrow L, Springer U, Fernandez H, Foote K, Okun M (2006) Startling facts about emotion in Parkinson’s disease: blunted reactivity to aversive stimuli. Brain 129(Pt 12):3356–3365

    Article  PubMed  Google Scholar 

  • Bradley MM, Lang PJ (2007) International affective digitized sounds, 2nd edn (IADS-2): affective ratings of sounds and instruction manual. Technical Report B-3 University of Florida, Gainesville, FL

  • Brown L, Grundlehner B, Penders J (2011) Towards wireless emotional valence detection from EEG. Proc IEEE Eng Med Biol Soc 2011:2188–2191. doi:10.1109/IEMBS.2011.6090412

  • Busk J, Galbraith GC (1975) EEG correlates of visual-motor practice in man. Electroencephalogr Clin Neurophysiol 38:415–422

    Article  CAS  PubMed  Google Scholar 

  • Caekebeke JF, Jennekens-Schinkel A, VanderLinden ME, Buruma OJ, Roos RA (1991) The interpretation of dysprosody in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 54(2):145–148

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cancelliere AEB, Kertesz A (1990) Lesion localization in acquired deficits of emotional expression and comprehension. Brain Cogn 13(2):133–147

    Article  CAS  PubMed  Google Scholar 

  • Celesia GG, Wanamaker WM (1972) Psychiatric disturbances in Parkinson’s disease. Dis Nerv Syst 33(9):577–583

    CAS  PubMed  Google Scholar 

  • Chen HL, Huang CC, Yu XG, Xu X, Sun X, Wang G, Wang SJ (2013) An efficient diagnosis system for detection of Parkinson’s disease using fuzzy k-nearest neighbor approach. Expert Syst Appl 40(1):263–271

    Article  Google Scholar 

  • Clark US, Neargarder S, Cronin-Golomb A (2008) Specific impairments in the recognition of emotional facial expressions in Parkinson’s disease. Neuropsychologia 46(9):2300–2309

    Article  PubMed Central  PubMed  Google Scholar 

  • Cohen H, Gagne M-H, Hess U, Pourcher E (2010) Emotion and object processing in Parkinson’s disease. Brain Cogn 72:457–463

    Article  PubMed  Google Scholar 

  • Cronin-Golomb A (2010) Parkinson’s disease as a disconnection syndrome. Neuropsychol Rev 20(2):191–208

    Article  PubMed Central  PubMed  Google Scholar 

  • Dara C, Monetta L, Pell MD (2008) Vocal emotion processing in Parkinson’s disease: reduced sensitivity to negative emotions. Brain Res 1188:100–111

    Article  CAS  PubMed  Google Scholar 

  • Davidson RJ (1992) Anterior cerebral asymmetry and the nature of emotion. Brain Cogn 20(1):125–151

    Article  CAS  PubMed  Google Scholar 

  • Dujardin K, Blairy S, Defebvre L, Duhem S, Noël Y, Hess U, Destée A (2004) Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia 42(2):239–250

    Article  PubMed  Google Scholar 

  • Fahn S, Elton RL, Committee M (1987) Unified Parkinson’s disease Rating Scale. In: Fahn’s, Marsden CD, Calne DB, Goldstein M, Clane DB (eds) Recent developments in Parkinson’s disease Macmillan health care information, Florham Park, vol 2, pp 153–163

  • Folstein MF, Folstein SE, Mchugh PR (1975) Mini-mental state examination: a practical method for grading the cognitive state of patients. Psychol Res 12(3):189–198

    Article  CAS  Google Scholar 

  • Fonseca LC, Tedrus GMAS, Carvas PN, Machado ECFA (2013) Comparison of quantitative EEG between patients with Alzheimer’s disease and those with Parkinson’s disease dementia. Clin Neurophysiol 124:1970–1974

    Article  PubMed  Google Scholar 

  • French CC, Beaumont JC (1984) A critical review of EEG coherence studies of hemisphere function. Int J Psychophysiol 1:241–254

    Article  CAS  PubMed  Google Scholar 

  • Garrido-Vásquez P, Pell MD, Paulmann S, Strecker K, Schwarz J, Kotz SA (2012) An ERP study of vocal emotion processing in asymmetric Parkinson’s disease. Soc Cogn Affect Neurosci 8(8):918–927

    Article  PubMed Central  PubMed  Google Scholar 

  • Gasser T, Jennen-Steinmetz C, Verleger R (1987) EEG coherence at rest and during a visual task in two groups of children. Electroencephalogr Clin Neurophysiol 67:151–158

    Article  CAS  PubMed  Google Scholar 

  • Gotlib IH, Raganathan C, Rosenfeld JP (1998) Frontal EEG alpha asymmetry, depression, and cognitive functioning. Cogn Emot 12(3):449–478

    Article  Google Scholar 

  • Gray HM, Tickle-Degnen L (2010) A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology 24(2):176–191

    Article  PubMed  Google Scholar 

  • Gross JJ, Levenson RW (1995) Emotion elicitation using films. Cogn Emot 9:87–108

    Article  Google Scholar 

  • Guevara MA, Corsi-Cabrera M (1996) EEG coherence or EEG correlation? Int J Psychophysiol 23(3):145–153

    Article  CAS  PubMed  Google Scholar 

  • Hadjidimitriou SK, Hadjileontiadis LJ (2012) Toward an EEG-based recognition of music liking using time-frequency analysis. IEEE Trans Biomed Eng 59(12):3498–3510

    Article  PubMed  Google Scholar 

  • Hamdi H, Richard P, Suteau A, Allain P (2012) Emotion assessment for affective computing based on physiological responses. In: IEEE proceedings of world congress on computational intelligence, pp 10–15

  • Hinrichs H, Machleidt W (1992) Basic emotions reflected in EEG-coherences. Int J Psychophysiol 13(3):225–232

    Article  CAS  PubMed  Google Scholar 

  • Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17(5):427–442

    Article  CAS  PubMed  Google Scholar 

  • Jerritta S, Murugappan M, Wan K, Yaacob S (2013) Electrocardiogram-based emotion recognition system using empirical mode decomposition and discrete Fourier transform. Expert Syst. doi:10.1111/exsy.12014

    Google Scholar 

  • Kan Y, Mimura M, Kamijima K, Kawamura M (2004) Recognition of emotion from moving facial and prosodic stimuli in depressed patients. J Neurol Neurosurg Psychiatry 75:1667–1671

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim J (2007) Bimodal emotion recognition using speech and physiological changes. Technical Report

  • Kim KH, Bang SW, Kim SR (2004) Emotion recognition system using short-term monitoring of physiological signal. Med Biol Eng Comput 42:419–427

    Article  CAS  PubMed  Google Scholar 

  • Kober H, Barrett LF, Joseph J, Bliss-Moreau E, Lindquist K, Wagera TD (2008) Functional grouping and cortical–subcortical interactions in emotion: a meta-analysis of neuroimaging studies. Neuroimage 42(2):998–1031

    Article  PubMed Central  PubMed  Google Scholar 

  • Lang PJ, Greenwald MK, Bradley MM, Hamm AO (1993) Looking at the pictures: affective, facial, visceral, and behavioral reactions. Psychophysiology 30(3):261–273

    Article  CAS  PubMed  Google Scholar 

  • Lawrence AD, Calder AJ, McGowan SW, Grasby PM (2002) Selective disruption of the recognition of facial expressions of anger. NeuroReport 13(6):881–884

    Article  PubMed  Google Scholar 

  • Lawrence AD, Goerendt IK, Brooks DJ (2007) Impaired recognition of facial expression of anger in Parkinson’s disease patients acutely withdrawn from dopamine replacement therapy. Neuropsychologia 45(1):65–74

    Article  PubMed  Google Scholar 

  • Leuchter AF, Newton TF, Cook IA, Walter DO, Rosenberg-Thompson S, Lachenbruch PA (1992) Changes in brain functional connectivity in Alzheimer-type and multi-infarct dementia. Brain 115(5):1543–1561

    Article  PubMed  Google Scholar 

  • Levin BE, Llabre MM, Weiner WJ (1989) Cognitive impairments associated with early Parkinson’s disease. Neurology 39(4):557–561

    Article  CAS  PubMed  Google Scholar 

  • Lima CF, Garrett C, Castro SL (2013) Not all the sounds sound the same: Parkinson’s disease affects differently emotion processing in music and in speech prosody. J Clin Exp Neuropsychol 35(4):373–392

    Article  PubMed  Google Scholar 

  • Lotze M, Reimold M, Heymans U, Laihinen A, Patt M, Halsband U (2009) Reduced ventrolateral fMRI response during observation of emotional gestures related to the degree of dopaminergic impairment in Parkinson disease. J Cogn Neurosci 21(7):1321–1331

    Article  PubMed  Google Scholar 

  • Madeley P, Ellis A, Mindham R (1995) Facial expressions and Parkinson’s disease. Behav Neurol 8(2):115–119

    Article  CAS  PubMed  Google Scholar 

  • Mikels J, Fredrickson B, Larkin G, Lindberg C, Maglio S, Reuter-Lorenz P (2005) Emotional category data on images from the international affective picture system. Behav Res Methods 37(4):630–636

    Article  Google Scholar 

  • Miller KM, Okun MS, Marsiske M, Fennell EB, Bowers D (2009) Startle reflex hyporeactivity in Parkinson’s disease: an emotion-specific or arousal-modulated deficit? Neuropsychologia 47:1917–1927

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mohr E, Juncos J, Cox C, Litvan I, Fedio P, Chase TN (1990) Selective deficits in cognition and memory in high-functioning Parkinsonian patients. J Neurol Neurosurg Psychiatry 53(7):603–606

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morita A, Kamei S, Serizawa K, Mizutani T (2009) The relationship between slowing EEGs and the progression of Parkinson’s disease. J Clin Neuropsychol 26(6):426–429

    Google Scholar 

  • Murugappan M, Rizon M, Nagarajan R, Yaacob S (2009) An investigation on visual and audiovisual stimulus based human emotion recognition using EEG. Int J Med Eng Inform 1(3):342–356

    Article  Google Scholar 

  • Neufeld MY, Inzelberg R, Korczyn AD (1988) EEG in demented and non-demented parkinsonian patients. Acta Neurol Scand 78(1):1–5

    Article  CAS  PubMed  Google Scholar 

  • Newton TF, Leuchter AF, Walter DO, Gorp WGV, Morgenstern H, Miller EN, Lieb K, Visscher B, Satz P, Weiner H (1994) Electroencephalographic coherence in acquired immune deficiency syndrome. Psychiatric Res 54(1):1–11

    Article  CAS  Google Scholar 

  • Nolte G, Bai O, Wheaton L, Mari Z, Vorbach S, Hallett M (2004) Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin Neurophysiol 115:2292–2307

    Article  PubMed  Google Scholar 

  • Obeso JA, Marin C, Rodriguez-Oroz C, Blesa J, Benitez-Temino B, Mena-Segovia J, Rodríguez M, Olanow CW (2008) The basal ganglia in Parkinson’s disease: current concepts and unexplained observations. Ann Neurol 64:S30–S46

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  PubMed  Google Scholar 

  • Paulmann S, Pell MD (2010) Dynamic emotion processing in Parkinson’s disease as a function of channel availability. J Clin Exp Neuropsychol 32(8):822–835

    Article  PubMed  Google Scholar 

  • Pell MD, Leonard CL (2003) Processing emotional tone from speech in Parkinson’s disease: a role for the basal ganglia. Cogn Affect Behav Neurosci 3(4):275–288

    Article  PubMed  Google Scholar 

  • Pell MD, Leonard CL (2005) Facial expression decoding in early Parkinson’s disease. Cogn Brain Res 23(3):327–340

    Article  Google Scholar 

  • Péron J, Dondaine T, Jeune FL, Grandjean D, Vérin M (2012) Emotional processing in Parkinson’s disease: a systematic review. Mov Disord 27(2):186–199

    Article  PubMed  Google Scholar 

  • Petrantonakis PC, Hadjileontiadis LJ (2011) A novel emotion elicitation index using frontal brain asymmetry for enhanced EEG-based emotion. IEEE Trans Inf Technol Biomed 15(5):737–746

    Article  PubMed  Google Scholar 

  • Pillon B, Dubois B, Agid Y (1996) Testing cognition may contribute to the diagnosis of movement disorders. Neurology 46(2):329–334

    Article  CAS  PubMed  Google Scholar 

  • Redondo J, Fraga I, Padron I, Pineiro A (2008) Affective ratings of sound stimuli. Behav Res Methods 40(3):784–790

    Article  PubMed  Google Scholar 

  • Roemer RA, Shagass C, Dubin W, Jaffe R, Siegal L (1992) Quantitative EEG in elderly depressives. Brain Topogr 4(4):285–290

    Article  CAS  PubMed  Google Scholar 

  • Salgado-Pineda P, Delaveau P, Blin O, Nieoullon A (2005) Dopaminergic contribution to the regulation of emotional perception. Clin Neuropharmacol 28(5):228–237

    Article  CAS  PubMed  Google Scholar 

  • Savitt JM, Dawson VL, Dawson TM (2006) Diagnosis and treatment of Parkinson disease: molecules to medicine. J Clin Investig 116(7):1744–1754

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schellberg D, Besthorn C, Klos T, Gasser T (1990) EEG power and coherence while male adults watch emotional video films. Int J Psychophysiol 9:279–291

    Article  CAS  PubMed  Google Scholar 

  • Schröder C, Möbes J, Schütze M, Szymanowski F, Nager W, Bangert M, Munte TF, Dengler R (2006) Perception of emotional speech in Parkinson’s disease. Mov Disord 21(10):1774–1778

    Article  PubMed  Google Scholar 

  • Sergerie K, Chochol C, Armony JL (2008) The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev 31:811–830

    Article  Google Scholar 

  • Shaw JC, O’Connor P, Ongley C (1977) The EEG as a measure of cerebral functional organization. Br J Psychiatry 130:260–264

    Article  CAS  PubMed  Google Scholar 

  • Soikkeli R, Partanen J, Soininen H, Paakkonen A, Riekkinen PS (1991) Slowing of EEG in Parkinson’s disease. Electroencephalogr Clin Neurophysiol 79(3):159–165

    Article  CAS  PubMed  Google Scholar 

  • Sprengelmeyer R, Young AW, Mahn K, Schroeder U, Woitalla D, Büttner T, Kuhn W, Przuntek H (2003) Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia 41(8):1047–1057

    Article  CAS  PubMed  Google Scholar 

  • Suzuki A, Hoshino T, Shigemasu K, Kawamura M (2006) Disgust-specific impairment of facial expression recognition in Parkinson’s disease. Brain 129(3):707–717

    Article  PubMed  Google Scholar 

  • Tessitore A, Hariri A, Fera F, Smith W, Chase T, Hyde T, Weinberger D, Mattay V (2002) Dopamine modulates the response of the human amygdala: a study in Parkinson’s disease. J Neurosci 22(20):9099–9103

    CAS  PubMed  Google Scholar 

  • Thatcher RW, Walker RA, Gerson I, Geisler FH (1989) EEG discriminant analyses of mild head trauma. Electroencephalogr Clin Neurophysiol 73(2):94–106

    Article  CAS  PubMed  Google Scholar 

  • Ventura MI, Baynes K, Sigvardt KA, Unruh AM, Acklin S, Kirsch HE, Disbrow EA (2012) Hemispheric asymmetries and prosodic emotion recognition deficits in Parkinson’s disease. Neuropsychologia 50:1936–1945

    Article  PubMed  Google Scholar 

  • Wang Y, Guan L (2008) Recognizing human emotional state from audiovisual signals. IEEE Trans Multimed 10(4):659–668

    Article  Google Scholar 

  • Wieser MJ, Muhlberger A, Alpers G, Macht M, Ellgring H, Pauli P (2006) Emotion processing in Parkinson’s disease: dissociation between early neuronal processing and explicit ratings. Clin Neurophysiol 117(1):94–102

    Article  PubMed  Google Scholar 

  • Wieser MJ, Klupp E, Weyers P, Pauli P, Weise D, Zeller D, Classen J, Muhlberger A (2012) Reduced early visual emotion discrimination as an index of diminished emotion processing in Parkinson’s disease?—evidence from event-related brain potentials. Cortex 48(9):1207–1217

    Article  PubMed  Google Scholar 

  • Yeager CL, Alberts WW, Denature LD (1966) Effect of stereotaxic surgery upon electroencephalographic status of parkinsonian patients. Neurology 16:904–910

    Article  Google Scholar 

  • Yip JT, Lee TM, Ho SL, Tsang KL, Li LS (2003) Emotion recognition in patients with idiopathic Parkinson’s disease. Mov Disord 18(10):1115–1122

    Article  PubMed  Google Scholar 

  • Yuvaraj R, Murugappan M, Norlinah MI, Sundaraj K, Khairiyah M (2013) Review of emotion recognition in stroke patients. Dement Geriatr Cogn Disord 36:179–196

    Article  PubMed  Google Scholar 

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Acknowledgments

The research was financially supported by Ministry of Science and Technology (MOSTI), Malaysia. Grant Number 9005-00053. The authors would like to thank Dr. Mohamad Fadli, Dr. Siva Rao Subramanian and Dr. Shahrul Azmin for their assistance with recruitment of PD participants. Also we would like to thank all of the individuals who participated in this study.

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Yuvaraj, R., Murugappan, M., Ibrahim, N.M. et al. Inter-hemispheric EEG coherence analysis in Parkinson’s disease: Assessing brain activity during emotion processing. J Neural Transm 122, 237–252 (2015). https://doi.org/10.1007/s00702-014-1249-4

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