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Brain Topography

, Volume 30, Issue 3, pp 333–342 | Cite as

The Effect of Lateralization of Motor Onset and Emotional Recognition in PD Patients Using EEG

Original Paper
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Abstract

The objective of this research was to investigate the relationship between emotion recognition and lateralization of motor onset in Parkinson’s disease (PD) patients using electroencephalogram (EEG) signals. The subject pool consisted of twenty PD patients [ten with predominantly left-sided (LPD) and ten with predominantly right-sided (RPD) motor symptoms] and 20 healthy controls (HC) that were matched for age and gender. Multimodal stimuli were used to evoke simple emotions, such as happiness, sadness, fear, anger, surprise, and disgust. Artifact-free emotion EEG signals were processed using the auto regressive spectral method and then subjected to repeated ANOVA measures. No group differences were observed across behavioral measures; however, a significant reduction in EEG spectral power was observed at alpha, beta and gamma frequency oscillations in LPD, compared to RPD and HC participants, suggesting that LPD patients (inferred right-hemisphere pathology) are impaired compared to RPD patients in emotional processing. We also found that PD-related emotional processing deficits may be selective to the perception of negative emotions. Previous findings have suggested a hemispheric effect on emotion processing that could be related to emotional response impairment in a subgroup of PD patients. This study may help in clinical practice to uncover potential neurophysiologic abnormalities of emotional changes with respect to PD patient’s motor onset.

Keywords

EEG Emotion Parkinson’s disease Body side of motor onset 

Notes

Acknowledgments

This research was financially supported by Fundamental Research Grant Scheme (FRGS), Ministry of Higher Education, Malaysia, Grant No: 9003-00507.

Compliance of Ethical Standards

Conflict of interest

The Author(s) declare(s) that there is no conflict of interest.

Supplementary material

10548_2016_524_MOESM1_ESM.docx (409 kb)
Supplementary material 1 (DOCX 409 kb)

References

  1. Adolphs R, Jansari A, Tranel D (2001) Hemispheric perception of emotional valence from facial expressions. Neuropsychology 15:516–524CrossRefPubMedGoogle Scholar
  2. Aftanas LI, Reva NV, Varlamov AA, Pavlov SV, Makhnev VP (2004) Analysis of evoked EEG synchronization and desynchronization in emotional activation in humans: temporal and topographic characteristics. Neurosci Behav Physiol 34:859–867CrossRefPubMedGoogle Scholar
  3. Akben SB, Subasi A, Tuncel D (2011) Analysis of EEG signals under flash stimulation for migraine and epileptic patients. J Med Syst 35:437–443CrossRefPubMedGoogle Scholar
  4. Ariatti A, Benuzzi F, Nichelli P (2008) Recognition of emotions from visual and prosodic cues in Parkinson’s disease. Neurol Sci 29:219–227CrossRefPubMedGoogle Scholar
  5. Balconi M, Lucchiari C (2008) Consciousness and arousal effects on emotional face processing as revealed by brain oscillations. A gamma band analysis. Int J Psychophysiol 67:41–46CrossRefPubMedGoogle Scholar
  6. Blonder LX, Gur RE, Gura RC (1989) The effects of right and left hemiparkinsonism on prosody. Brain Lang 36:193–207CrossRefPubMedGoogle Scholar
  7. Clark US, Neargarder S, Cronin-Golomb A (2008) Specific impairments in the recognition of emotional facial expressions in Parkinson’s disease. Neuropsychologia 46:2300–2309CrossRefPubMedPubMedCentralGoogle Scholar
  8. Dara C, Monetta L, Pell MD (2008) Vocal emotion processing in Parkinson’s disease: reduced sensitivity to negative emotions. Brain Res 1188:100–111CrossRefPubMedGoogle Scholar
  9. 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, 2nd edn. Macmillan Health Care Information, Florham Park, pp 153–163Google Scholar
  10. Garrido-Vásquez P, Pell MD, Paulmann S, Strecker K, Schwarz J, Kotz SA (2013) An ERP study of vocal emotion processing in asymmetric Parkinson’s disease. Soc Cogn Affect Neurosci 8:918–927CrossRefPubMedGoogle Scholar
  11. Gotlib IH, Raganathan C, Rosenfeld JP (1998) Frontal EEG alpha asymmetry, depression, and cognitive functioning. Cogn Emotion 12:449–478CrossRefGoogle Scholar
  12. Gray HM, Tickle-Degnen L (2010) A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology 24:176–191CrossRefPubMedGoogle Scholar
  13. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442CrossRefPubMedGoogle Scholar
  14. 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 75:1667–1671CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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 35:373–392CrossRefPubMedGoogle Scholar
  16. Lin YP, Yang YH, Jung TP (2014) Fusion of electroencephalographic dynamics and musical contents for estimating emotional responses in music listening. Front Neurosci 8:1–14Google Scholar
  17. Luo Q, Holroyd T, Jones M, Hendler T, Blair J (2007) Neural dynamics for facial threat processing as revealed by gamma band synchronization using MEG. Neuroimage 34:839–847CrossRefPubMedGoogle Scholar
  18. Mikutta C, Altorfer A, Strik W, Koenig T (2012) Emotions, arousal, and frontal alpha rhythm asymmetry during Beethoven’s 5th symphony. Brain Topogr 25:423–430CrossRefPubMedGoogle Scholar
  19. Neufeld MY, Inzelberg R, Korczyn AD (1988) EEG in demented and non-demented parkinsonian patients. Acta Neurol Scand 78:1–5CrossRefPubMedGoogle Scholar
  20. Pell MD, Baum SR (1997) Unilateral brain damage, prosodic comprehension deficits, and the acoustic cues to prosody. Brain Lang 57:195–214CrossRefPubMedGoogle Scholar
  21. Pell MD, Leonard CL (2003) Processing emotional tone from speech in Parkinson’s disease: a role for the basal ganglia. Cogn Affect Behav Neurosci 3:275–288CrossRefPubMedGoogle Scholar
  22. Péron J, Dondaine T, Jeune FL, Grandjean D, Vérin M (2012) Emotional processing in Parkinson’s disease: a systematic review. Mov Disord 27:186–199CrossRefPubMedGoogle Scholar
  23. Petrantonakis PC, Hadjileontiadis LJ (2010) Emotion recognition from brain signals using hybrid adaptive filtering and higher order crossings analysis. IEEE Trans Affect Comput 1:81–96CrossRefGoogle Scholar
  24. Salgado-Pineda P, Delaveau P, Blin O, Nieoullon A (2005) Dopaminergic contribution to the regulation of emotional perception. Clin Neuropharmacol 28:228–237CrossRefPubMedGoogle Scholar
  25. Sammler D, Grigutsch M, Fritz T, Koelsch S (2007) Music and emotion: electrophysiological correlates of the processing of pleasant and unpleasant music. Psychophysiology 44:293–304CrossRefPubMedGoogle Scholar
  26. Sarlo M, Buodo G, Poli S, Palomba D (2005) Changes in EEG alpha power to different disgust elicitors: the specificity of mutilations. Neurosci Lett 382:291–296CrossRefPubMedGoogle Scholar
  27. Schröder C et al (2006) Perception of emotional speech in Parkinson’s disease. Mov Disord 21:1774–1778CrossRefPubMedGoogle Scholar
  28. Tessitore A et al (2002) Dopamine modulates the response of the human amygdala: a study in Parkinson’s disease. J Neurosci 22:9099–9103PubMedGoogle Scholar
  29. VanLancker D, Sidtis JJ (1992) The identification of affective, prosodic stimuli by left and right -hemisphere damaged subjects: all errors are not created equal. J Speech Hear Res 35:963–970CrossRefGoogle Scholar
  30. 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 50:1936–1945CrossRefPubMedGoogle Scholar
  31. Wang XW, Nie D, Lu BL (2013) Emotional state classification from EEG data using machine learning approach. Neurocomputing 129:94–106. doi: 10.1016/j.neucom.2013.06.046 CrossRefGoogle Scholar
  32. 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 117:94–102CrossRefPubMedGoogle Scholar
  33. Yip JT, Lee TM, Ho SL, Tsang KL, Li LS (2003) Emotion recognition in patients with idiopathic Parkinson’s disease. Mov Disord 18:1115–1122CrossRefPubMedGoogle Scholar
  34. Yuvaraj R, Murugappan M, Norlinah MI, Sundaraj K, Khairiyah M (2013a) Review of emotion recognition in stroke patients. Dement Geriatr Cogn Disord 36:179–196CrossRefPubMedGoogle Scholar
  35. Yuvaraj R, Murugappan M, Omar MI, Norlinah MI, Sundaraj K, Khairiyah M, Satiyan M (2013b) Emotion processing in Parkinson’s disease: an EEG spectral power study. Int J Neurosci 124:491–502CrossRefPubMedGoogle Scholar
  36. Yuvaraj R et al (2014a) On the analysis of EEG power, frequency and asymmetry in Parkinson’s disease during emotion processing. Behav Brain Funct 10:1–19CrossRefGoogle Scholar
  37. Yuvaraj R et al (2014b) Inter-hemispheric EEG coherence analysis in Parkinson’s disease: assessing brain activity during emotion processing. J Neural Transm 122:237–252CrossRefPubMedGoogle Scholar
  38. Yuvaraj R, Murugappan M, Norlinah MI, Sundaraj K, Omar MI, Khairiyah M, Palaniappan R (2014c) Optimal set of EEG features for emotional state classification and trajectory visualization in Parkinson’s disease. Int J Psychophysiol 94:482–495CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringSri Sivasubramaniya Nadar (SSN) College of EngineeringChennaiIndia
  2. 2.Department of Electronics and Communication EngineeringKuwait College of Science and TechnologySafatKuwait
  3. 3.School of ComputingUniversity of KentMedwayUK
  4. 4.Neural Systems Laboratory, Department of Biomedical EngineeringUniversity of KentuckyLexingtonUSA

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