Skip to main content
Log in

Analysis of functional brain connections for positive–negative emotions using phase locking value

  • Research Article
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

Abstract

In this study, we investigate the brain networks during positive and negative emotions for different types of stimulus (audio only, video only and audio + video) in \(\alpha , \beta\), and \(\gamma\) bands in terms of phase locking value, a nonlinear method to study functional connectivity. Results show notable hemispheric lateralization as phase synchronization values between channels are significant and high in right hemisphere for all emotions. Left frontal electrodes are also found to have control over emotion in terms of functional connectivity. Besides significant inter-hemisphere phase locking values are observed between left and right frontal regions, specifically between left anterior frontal and right mid-frontal, inferior-frontal and anterior frontal regions; and also between left and right mid frontal regions. ANOVA analysis for stimulus types show that stimulus types are not separable for emotions having high valence. PLV values are significantly different only for negative emotions or neutral emotions between audio only/video only and audio only/audio + video stimuli. Finding no significant difference between video only and audio + video stimuli is interesting and might be interpreted as that video content is the most effective part of a stimulus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Adolphs R (2002) Recognizing emotion from facial expressions: psychological and neurological mechanisms. Behav Cogn Neurosci Rev 1(1):21–62

    Article  PubMed  Google Scholar 

  • Alfano KM, Cimino CR (2008) Alteration of expected hemispheric asymmetries: valence and arousal effects in neuropsychological models of emotion. Brain Cogn 66(3):213–220

    Article  PubMed  Google Scholar 

  • Badcock NA, Mousikou P, Mahajan Y, deLissa P, Thie J, McArthur G (2013) Validation of the Emotiv EPOC® EEG gaming system for measuring research quality auditory ERPs. PeerJ 1:e38

    Article  PubMed  PubMed Central  Google Scholar 

  • Balconi M, Lucchiari C (2006) EEG correlates (event-related desynchronization) of emotional face elaboration: a temporal analysis. Neurosci Lett 392(1):118–123

    Article  CAS  PubMed  Google Scholar 

  • 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(1):41–46

    Article  PubMed  Google Scholar 

  • Balconi M, Mazza G (2009) Brain oscillations and bis/bas (behavioral inhibition/activation system) effects on processing masked emotional cues: Ers/erd and coherence measures of alpha band. Int J Psychophysiol 74(2):158–165

    Article  PubMed  Google Scholar 

  • Başar E, Güntekin B (2012) A short review of alpha activity in cognitive processes and in cognitive impairment. Int J Psychophysiol 86(1):25–38

    Article  PubMed  Google Scholar 

  • Baumgartner T, Esslen M, Jäncke 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 

  • Bobrov P, Frolov A, Cantor C, Fedulova I, Bakhnyan M, Zhavoronkov A (2011) Brain–computer interface based on generation of visual images. PLoS ONE 6(6):e20674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonita JD, Ambolode LCC, Rosenberg BM, Cellucci CJ, Watanabe TAA, Rapp PE, Albano AM (2014) Time domain measures of inter-channel eeg correlations: a comparison of linear, nonparametric and nonlinear measures. Cogn Neurodyn 8(1):1–15

    Article  CAS  PubMed  Google Scholar 

  • Borod JC, Obler LK, Agosti RM, Borod JC, Santschi C (1998) Right hemisphere emotional perception: evidence across multiple channels. Neuropsychology 12(3):446–458

    Article  CAS  PubMed  Google Scholar 

  • Bradley MM, Lang PJ (1994) Measuring emotion: the self-assessment manikin and the semantic differential. J Behav Therapy Exp Psychiatry 25(1):49–59

    Article  CAS  Google Scholar 

  • Bressler SL (1995) Large-scale cortical networks and cognition. Brain Res Rev 20:288–304

    Article  CAS  PubMed  Google Scholar 

  • Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler SL (2004) Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc Natl Acad Sci USA 101(26):9849–9854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y-H, Christopher Edgar J, Holroyd T, Dammers J, Thönneßen H, Roberts TPL, Mathiak K (2010) Neuromagnetic oscillations to emotional faces and prosody. Eur J Neurosci 31(10):1818–1827

    Article  PubMed  Google Scholar 

  • Del Zotto M, Deiber M-P, Legrand LB, De Gelder B, Pegna AJ (2013) Emotional expressions modulate low \(\alpha\) and \(\beta\) oscillations in a cortically blind patient. Int J Psychophysiol 90(3):358–362

    Article  PubMed  Google Scholar 

  • Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134(1):9–21

    Article  PubMed  Google Scholar 

  • Dimitriadis SI, Laskaris NA, Micheloyannis S (2015) Transition dynamics of eeg-based network microstates during mental arithmetic and resting wakefulness reflects task-related modulations and developmental changes. Cogn Neurodyn 9(4):371–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding M, Bressler SL, Yang W, Liang H (2000) Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: data preprocessing, model validation, and variability assessment. Biol Cybern 83(1):35–45

    Article  CAS  PubMed  Google Scholar 

  • Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck H (1988) Coherent oscillations: a mechanism of feature linking in the visual cortex? Biol Cybern 60(2):121–130

    Article  CAS  PubMed  Google Scholar 

  • Engel AK, Fries P (2010) Beta-band oscillationssignalling the status quo? Curr Opin Neurobiol 20(2):156–165

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Herrero G (2007) Automatic artifact removal (AAR) toolbox v1.3 for MATLAB. Tamp Univ Technol 3:1–23

    Google Scholar 

  • Güntekin B, Basar E (2007) Emotional face expressions are differentiated with brain oscillations. Int J Psychophysiol 64(1):91–100

    Article  PubMed  Google Scholar 

  • Güntekin B, Başar E (2014) A review of brain oscillations in perception of faces and emotional pictures. Neuropsychologia 58:33–51

    Article  PubMed  Google Scholar 

  • Harmon-Jones E (2003) Clarifying the emotive functions of asymmetrical frontal cortical activity. Psychophysiology 40(6):838–848

    Article  PubMed  Google Scholar 

  • Hassan M, Wendling F (2015) Tracking dynamics of functional brain networks using dense eeg. IRBM 36(6):324–328

    Article  Google Scholar 

  • Hassan M, Benquet P, Biraben A, Berrou C, Dufor O, Wendling F (2015) Dynamic reorganization of functional brain networks during picture naming. Cortex 73:276–288

    Article  PubMed  Google Scholar 

  • Hattingh CJ, Ipser J, Tromp S, Syal S, Lochner C, Brooks SJB, Stein DJ (2013) Functional magnetic resonance imaging during emotion recognition in social anxiety disorder: an activation likelihood meta-analysis. Front Hum Neurosci 6:347

    Article  PubMed  PubMed Central  Google Scholar 

  • Holmes A, Vuilleumier P, Eimer M (2003) The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials. Cogn Brain Res 16(2):174–184

    Article  Google Scholar 

  • Holtgraves T, Felton A (2011) Hemispheric asymmetry in the processing of negative and positive words: a divided field study. Cogn Emot 25(4):691–699

    Article  PubMed  Google Scholar 

  • Hooker CI, Hooker CI, Bruce L, Fisher M, Verosky SC, Miyakawa A, Vinogradov S (2012) Neural activity during emotion recognition after combined cognitive plus social cognitive training in schizophrenia. Schizophr Res 139(1):53–59

    Article  PubMed  PubMed Central  Google Scholar 

  • Iwaki T, Noshiro M (2012) Eeg activity over frontal regions during positive and negative emotional experience. In: 2012 ICME international conference on complex medical engineering (CME), pp 418–422

  • Jabbi M, Kohn PD, Nash T, Ianni A, Coutlee C, Holroyd T, Carver FW, Chen Q, Cropp B, Kippenhan JS et al (2014) Convergent bold and beta-band activity in superior temporal sulcus and frontolimbic circuitry underpins human emotion cognition. Cereb Cortex bht427

  • Jatupaiboon N, Pan-ngum S, Israsena P (2013) Real-time eeg-based happiness detection system. Sci World J. doi:10.1155/2013/618649

    Article  Google Scholar 

  • Joczyk R (2016) Hemispheric asymmetry of emotion words in a non-native mind: a divided visual field study. Laterality Asymmetries Body Brain Cogn 20(3):326–347

    Article  Google Scholar 

  • Kang J-S, Park U, Gonuguntla V, Veluvolu KC, Lee M (2015) Human implicit intent recognition based on the phase synchrony of EEG signals. Pattern Recognit Lett 66:144–152

    Article  Google Scholar 

  • Kassam KS, Markey AR, Cherkassky VL, Loewenstein G, Just MA (2013) Identifying emotions on the basis of neural activation. PLoS ONE 8(6):e66032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keil A, Müller MM, Gruber T, Wienbruch C, Stolarova M, Elbert T (2001) Effects of emotional arousal in the cerebral hemispheres: a study of oscillatory brain activity and event-related potentials. Clin Neurophysiol 112(11):2057–2068

    Article  CAS  PubMed  Google Scholar 

  • Khosrowabadi R, Heijnen M, Wahab A, Quek HC (2010) The dynamic emotion recognition system based on functional connectivity of brain regions. In: 2010 IEEE intelligent vehicles symposium (IV). IEEE, pp 377–381

  • Koelstra S, Mühl C, Soleymani M, Lee JS, Yazdani A, Ebrahimi T, Pun T, Nijholt A, Patras I (2012) DEAP: a database for emotion analysis; using physiological signals. IEEE Trans Affect Comput 3(1):18–31

    Article  Google Scholar 

  • Konigqt P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157

    Article  Google Scholar 

  • Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8(4):194–208

    Article  CAS  PubMed  Google Scholar 

  • Lachaux J-P, Rodriguez E, Le Van Quyen M, Lutz A, Martinerie J, Varela FJ (2000) Studying single-trials of phase synchronous activity in the brain. Int J Bifurc Chaos 10(10):2429–2439

    Article  Google Scholar 

  • Lane RD, Nadel L (2002) Cognitive neuroscience of emotion. Oxford University Press, Oxford

    Google Scholar 

  • Le Van Quyen M, Foucher J, Lachaux J, Rodriguez E, Lutz A, Martinerie J, Varela FJ (2001) Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony. J Neurosci Methods 111(2):83–98

    Article  Google Scholar 

  • Lee Y-Y, Hsieh S (2014) Classifying different emotional states by means of EEG-based functional connectivity patterns. PloS ONE 9(4):e95415

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Y, Cao D, Wei L, Tang Y, Wang J (2015) Abnormal functional connectivity of eeg gamma band in patients with depression during emotional face processing. Clin Neurophysiol 126(11):2078–2089

    Article  PubMed  Google Scholar 

  • Lichev V, Sacher J, Ihme K, Rosenberg N, Quirin M, Lepsien J, Pampel A, Rufer M, Grabe H-J, Kugel H et al (2015) Automatic emotion processing as a function of trait emotional awareness: an fMRI study. Soc Cogn Affect Neurosci 10(5):680–689

    Article  PubMed  Google Scholar 

  • Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Barrett LF (2012) The brain basis of emotion: a meta-analytic review. Behav Brain Sci 35(03):121–143

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y-J, Yu M, Zhao G, Song J, Ge Y, Shi Y (2017) Real-time movie-induced discrete emotion recognition from EEG signals. IEEE Trans Affect Comput. doi:10.1109/TAFFC.2017.2660485

    Google Scholar 

  • 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(2):839–847

    Article  PubMed  Google Scholar 

  • Luo Q, Mitchell D, Cheng X, Mondillo K, Mccaffrey D, Holroyd T, Carver F, Coppola R, Blair J (2009) Visual awareness, emotion, and gamma band synchronization. Cereb Cortex 19(8):1896–1904

    Article  PubMed  Google Scholar 

  • Ma M, Li Y, Xu Z, Tang Y, Wang J (2012) Small-world network organization of functional connectivity of EEG gamma oscillation during emotion-related processing. In: 2012 5th International conference on biomedical engineering and informatics (BMEI). IEEE, pp 597–600

  • Mashal N, Itkes O (2016) The effects of emotional valence on hemispheric processing of metaphoric word pairs. Laterality Asymmetries Body Brain Cogn 19(5):511–521

    Article  Google Scholar 

  • McAuley J, Marsden C (2000) Physiological and pathological tremors and rhythmic central motor control. Brain 123(8):1545–1567

    Article  PubMed  Google Scholar 

  • McMahan T, Parberry I, Parsons TD (2015) Modality specific assessment of video game players experience using the Emotiv. Entertain Comput 7:1–6

    Article  Google Scholar 

  • Mitchell RLC, Elliott R, Barry M, Cruttenden A, Woodruff PWR (2003) The neural response to emotional prosody, as revealed by functional magnetic resonance imaging. Neuropsychologia 41:1410–1421

    Article  PubMed  Google Scholar 

  • Mormann F, Lehnertz K, David P, Elger CE (2000) Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Phys D Nonlinear Phenom 144(3):358–369

    Article  Google Scholar 

  • Morris JS, Frith CD, Perrett DI, Rowland D et al (1996) A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383(6603):812

    Article  CAS  PubMed  Google Scholar 

  • Murthy VN, Fetz EE (1992) Coherent 25-to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci 89(12):5670–5674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müsch K, Hamamé CM, Perrone-Bertolotti M, Minotti L, Kahane P, Engel AK, Lachaux J-P, Schneider TR (2014) Selective attention modulates high-frequency activity in the face-processing network. Cortex 60:34–51

    Article  PubMed  Google Scholar 

  • Nunez PL, Srinivasan R, Westdorp F, Wijesinghe RS, Tucker DM, Silberstein RB, Cadusch PJ (1997) EEG coherency. I: statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. Electroencephalogr Clin Neurophysiol 103(5):499–515

    Article  CAS  PubMed  Google Scholar 

  • Palermo R, Rhodes G (2007) Are you always on my mind? A review of how face perception and attention interact. Neuropsychologia 45(1):75–92

    Article  PubMed  Google Scholar 

  • Pizzagalli D, Regard M, Lehmann D (1999) Rapid emotional face processing in the human right and left brain hemispheres: an ERP study. Neuroreport 10(13):2691–2698

    Article  CAS  PubMed  Google Scholar 

  • Popov T, Miller GA, Rockstroh B, Weisz N (2013) Modulation of \(\alpha\) power and functional connectivity during facial affect recognition. J Neurosci 33(14):6018–6026

    Article  CAS  PubMed  Google Scholar 

  • Quraan MA, Protzner AB, Daskalakis ZJ, Giacobbe P, Tang CW, Kennedy SH, Lozano AM, McAndrews MP (2014) EEG power asymmetry and functional connectivity as a marker of treatment effectiveness in DBS surgery for depression. Neuropsychopharmacology 39(5):1270–1281

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodríguez A, Rey B, Clemente M, Wrzesien M, Alcañiz M (2015) Assessing brain activations associated with emotional regulation during virtual reality mood induction procedures. Expert Syst Appl 42(3):1699–1709

    Article  Google Scholar 

  • Sakkalis V (2011) Review of advanced techniques for the estimation of brain connectivity measured with EEG/MEG. Comput Biol Med 41(12):1110–1117

    Article  CAS  PubMed  Google Scholar 

  • Salenius S, Hari R (2003) Synchronous cortical oscillatory activity during motor action. Curr Opin Neurobiol 13(6):678–684

    Article  CAS  PubMed  Google Scholar 

  • Sato W, Kochiyama T, Uono S, Matsuda K, Usui K, Inoue Y, Toichi M (2011) Rapid amygdala gamma oscillations in response to fearful facial expressions. Neuropsychologia 49(4):612–617

    Article  PubMed  Google Scholar 

  • Schoenberg PLA, Speckens AEM (2015) Multi-dimensional modulations of \(\alpha\) and \(\gamma\) cortical dynamics following mindfulness-based cognitive therapy in major depressive disorder. Cogn Neurodyn 9(1):13–29

    Article  PubMed  Google Scholar 

  • Shahabi H, Moghimi S (2016) Toward automatic detection of brain responses to emotional music through analysis of EEG effective connectivity. Comput Hum Behav 58:231–239

    Article  Google Scholar 

  • Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18(1):555–586

    Article  CAS  PubMed  Google Scholar 

  • Stam CJ, van Dijk BW (2002) Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets. Phys D Nonlinear Phenom 163(3–4):236–251

    Article  Google Scholar 

  • Steyn-Ross ML, Steyn-Ross DA, Sleigh JW (2012) Gap junctions modulate seizures in a mean-field model of general anesthesia for the cortex. Cogn Neurodyn 6(3):215–225

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun J, Hong X, Tong S (2012) Phase synchronization analysis of EEG signals: an evaluation based on surrogate tests. IEEE Trans Biomed Eng 59(8):2254–2263

    Article  Google Scholar 

  • Symons AE, El-Deredy W, Schwartze M, Kotz SA (2016) The functional role of neural oscillations in non-verbal emotional communication. Front Hum Neurosci. doi:10.3389/fnhum.2016.00239

    PubMed  PubMed Central  Google Scholar 

  • Tass P, Rosenblum MG, Weule J, Kurths J, Pikovsky A, Volkmann J, Schnitzler A, Freund H-J (1998) Detection of n:m phase locking from noisy data: application to magnetoencephalography. Phys Rev Lett 81(15):3291

    Article  CAS  Google Scholar 

  • Tripathy D, Raheja JL (2015) Design and implementation of brain computer interface based robot motion control. In: Proceedings of the 3rd international conference on frontiers of intelligent computing: theory and applications (FICTA) 2014, vol 328. Springer, Berlin, pp 289–296

  • Tucker D, Roth D, Bair T (1986) Functional connections among cortical regions: topography of EEG coherence. Electroencephalogr Clin Neurophysiol 63(3):242–250

    Article  CAS  PubMed  Google Scholar 

  • Wilmer A, de Lussanet MHE, Lappe M (2010) A method for the estimation of functional brain connectivity from time-series data. Cogn Neurodyn 4(2):133–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winkler I, Haufe S, Tangermann M (2011) Automatic classification of artifactual ICA-components for artifact removal in EEG signals. Behav Brain Funct 7(1):30

    Article  PubMed  PubMed Central  Google Scholar 

  • Yener GG, Başar E (2010) Sensory evoked and event related oscillations in alzheimers disease: a short review. Cogn Neurodyn 4(4):263–274

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu H, Sunderraj CMAA, Chang CK, Wong J (2015) Emotion aware system for the elderly. Smart homes and health telematics. Springer, Berlin, pp 175–183

  • Zion-Golumbic E, Kutas M, Bentin S (2010) Neural dynamics associated with semantic and episodic memory for faces: evidence from multiple frequency bands. J Cogn Neurosci 22(2):263–277

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasar Dasdemir.

Appendix

Appendix

Insignificant channels

Insignificant channel pairs after performing permutation test with 1000 surrogate values are shown in Table 5. Significance level is set to \(\alpha =0.01\). In the table, corresponding p values and PLV values are shown below the channel pair.

Number of trials

PLVs are calculated for each electrode pair by averaging across trials which have the same properties; same stimulus type (audio, video, audio + video), same emotion (positive, negative, neutral) for each oscillation (\(\alpha , \beta , \gamma\)). Number of EEG segments collected from all subjects for each condition pair is given in Table 6.

Table 6 Number of stimulus for different conditions

Single trial phase locking values (S-PLV) are calculated for each condition, in order to generate the PLV distributions for ANOVA analysis. S-PLV definition is defined in Lachaux et al. (2000) and shown in Eq. 4.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dasdemir, Y., Yildirim, E. & Yildirim, S. Analysis of functional brain connections for positive–negative emotions using phase locking value. Cogn Neurodyn 11, 487–500 (2017). https://doi.org/10.1007/s11571-017-9447-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-017-9447-z

Keywords

Navigation