Electrophysiological Correlates of Vocal Emotional Processing in Musicians and Non-Musicians
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.1.1. Musicians
2.1.2. Non-Musicians
2.2. Stimuli
2.2.1. Original Audio Recordings
2.2.2. Parameter-Specific Voice Morphing
2.3. Design
2.3.1. EEG Setup
2.3.2. Procedure
2.4. Data Processing
2.5. Statistical Analysis
3. Results
3.1. Comparability of Musicians and Non-Musicians: Demography, Personality, and Musicality
3.2. Behavioral Data
3.3. ERP
3.3.1. P200
3.3.2. N400
3.3.3. LPP
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Banse, R.; Scherer, K.R. Acoustic profiles in vocal emotion expression. J. Pers. Soc. Psychol. 1996, 70, 614–636. [Google Scholar] [CrossRef] [PubMed]
- Juslin, P.N.; Laukka, P. Communication of emotions in vocal expression and music performance: Different channels, same code? Psychol. Bull. 2003, 129, 770–814. [Google Scholar] [CrossRef] [PubMed]
- Scherer, K.R. Acoustic Patterning of Emotion Vocalizations. In The Oxford Handbook of Voice Perception; Frühholz, S., Belin, P., Frühholz, S., Belin, P., Scherer, K.R., Eds.; Oxford University Press: Oxford, UK, 2018; pp. 60–92. ISBN 9780198743187. [Google Scholar]
- Frühholz, S.; Trost, W.; Kotz, S.A. The sound of emotions—Towards a unifying neural network perspective of affective sound processing. Neurosci. Biobehav. Rev. 2016, 68, 96–110. [Google Scholar] [CrossRef] [PubMed]
- Paulmann, S.; Kotz, S.A. The Electrophysiology and Time Course of Processing Vocal Emotion Expressions. In The Oxford Handbook of Voice Perception; Frühholz, S., Belin, P., Frühholz, S., Belin, P., Scherer, K.R., Eds.; Oxford University Press: Oxford, UK, 2018; pp. 458–472. ISBN 9780198743187. [Google Scholar]
- Schirmer, A.; Kotz, S.A. Beyond the right hemisphere: Brain mechanisms mediating vocal emotional processing. Trends Cogn. Sci. 2006, 10, 24–30. [Google Scholar] [CrossRef]
- Liu, T.; Pinheiro, A.P.; Deng, G.; Nestor, P.G.; McCarley, R.W.; Niznikiewicz, M.A. Electrophysiological insights into processing nonverbal emotional vocalizations. Neuroreport 2012, 23, 108–112. [Google Scholar] [CrossRef]
- Pinheiro, A.P.; Del Re, E.; Mezin, J.; Nestor, P.G.; Rauber, A.; McCarley, R.W.; Gonçalves, Ó.F.; Niznikiewicz, M.A. Sensory-based and higher-order operations contribute to abnormal emotional prosody processing in schizophrenia: An electrophysiological investigation. Psychol. Med. 2013, 43, 603–618. [Google Scholar] [CrossRef]
- Schirmer, A.; Escoffier, N. Emotional MMN: Anxiety and heart rate correlate with the ERP signature for auditory change detection. Clin. Neurophysiol. 2010, 121, 53–59. [Google Scholar] [CrossRef]
- Schirmer, A.; Chen, C.-B.; Ching, A.; Tan, L.; Hong, R.Y. Vocal emotions influence verbal memory: Neural correlates and interindividual differences. Cogn. Affect. Behav. Neurosci. 2013, 13, 80–93. [Google Scholar] [CrossRef]
- Paulmann, S.; Kotz, S.A. Early emotional prosody perception based on different speaker voices. Neuroreport 2008, 19, 209–213. [Google Scholar] [CrossRef]
- Paulmann, S.; Bleichner, M.; Kotz, S.A. Valence, arousal, and task effects in emotional prosody processing. Front. Psychol. 2013, 4, 345. [Google Scholar] [CrossRef]
- Nussbaum, C.; Schirmer, A.; Schweinberger, S.R. Contributions of fundamental frequency and timbre to vocal emotion perception and their electrophysiological correlates. Soc. Cogn. Affect. Neurosci. 2022, 17, 1145–1154. [Google Scholar] [CrossRef] [PubMed]
- Schirmer, A.; Striano, T.; Friederici, A.D. Sex differences in the preattentive processing of vocal emotional expressions. Neuroreport 2005, 16, 635–639. [Google Scholar] [CrossRef]
- Arias, P.; Rachman, L.; Liuni, M.; Aucouturier, J.-J. Beyond Correlation: Acoustic Transformation Methods for the Experimental Study of Emotional Voice and Speech. Emot. Rev. 2021, 13, 12–24. [Google Scholar] [CrossRef]
- Schirmer, A.; Kotz, S.A. ERP evidence for a sex-specific Stroop effect in emotional speech. J. Cogn. Neurosci. 2003, 15, 1135–1148. [Google Scholar] [CrossRef] [PubMed]
- Schirmer, A.; Kotz, S.A.; Friederici, A.D. On the role of attention for the processing of emotions in speech: Sex differences revisited. Cogn. Brain Res. 2005, 24, 442–452. [Google Scholar] [CrossRef] [PubMed]
- Nussbaum, C.; Schweinberger, S.R. Links between Musicality and Vocal Emotion Perception. Emot. Rev. 2021, 13, 211–224. [Google Scholar] [CrossRef]
- Martins, M.; Pinheiro, A.P.; Lima, C.F. Does Music Training Improve Emotion Recognition Abilities? A Critical Review. Emot. Rev. 2021, 13, 199–210. [Google Scholar] [CrossRef]
- Thompson, W.F.; Schellenberg, E.G.; Husain, G. Decoding speech prosody: Do music lessons help? Emotion 2004, 4, 46–64. [Google Scholar] [CrossRef]
- Lima, C.F.; Castro, S.L. Speaking to the trained ear: Musical expertise enhances the recognition of emotions in speech prosody. Emotion 2011, 11, 1021–1031. [Google Scholar] [CrossRef]
- Globerson, E.; Amir, N.; Golan, O.; Kishon-Rabin, L.; Lavidor, M. Psychoacoustic abilities as predictors of vocal emotion recognition. Atten. Percept. Psychophys. 2013, 75, 1799–1810. [Google Scholar] [CrossRef]
- Lima, C.F.; Brancatisano, O.; Fancourt, A.; Müllensiefen, D.; Scott, S.K.; Warren, J.D.; Stewart, L. Impaired socio-emotional processing in a developmental music disorder. Sci. Rep. 2016, 6, 34911. [Google Scholar] [CrossRef]
- Thompson, W.F.; Marin, M.M.; Stewart, L. Reduced sensitivity to emotional prosody in congenital amusia rekindles the musical protolanguage hypothesis. Proc. Natl. Acad. Sci. USA 2012, 109, 19027–19032. [Google Scholar] [CrossRef]
- Correia, A.I.; Castro, S.L.; MacGregor, C.; Müllensiefen, D.; Schellenberg, E.G.; Lima, C.F. Enhanced recognition of vocal emotions in individuals with naturally good musical abilities. Emotion 2022, 22, 894–906. [Google Scholar] [CrossRef] [PubMed]
- Kraus, N.; Chandrasekaran, B. Music training for the development of auditory skills. Nat. Rev. Neurosci. 2010, 11, 599–605. [Google Scholar] [CrossRef]
- Elmer, S.; Dittinger, E.; Besson, M. One Step Beyond—Musical Expertise and Word Learning. In The Oxford Handbook of Voice Perception; Frühholz, S., Belin, P., Frühholz, S., Belin, P., Scherer, K.R., Eds.; Oxford University Press: Oxford, UK, 2018; pp. 208–234. ISBN 9780198743187. [Google Scholar]
- Lolli, S.L.; Lewenstein, A.D.; Basurto, J.; Winnik, S.; Loui, P. Sound frequency affects speech emotion perception: Results from congenital amusia. Front. Psychol. 2015, 6, 1340. [Google Scholar] [CrossRef]
- Nussbaum, C.; Schirmer, A.; Schweinberger, S.R. Musicality—Tuned to the melody of vocal emotions. Br. J. Psychol. 2023; online ahead of print. [Google Scholar] [CrossRef]
- Pantev, C.; Herholz, S.C. Plasticity of the human auditory cortex related to musical training. Neurosci. Biobehav. Rev. 2011, 35, 2140–2154. [Google Scholar] [CrossRef]
- Chartrand, J.-P.; Peretz, I.; Belin, P. Auditory recognition expertise and domain specificity. Brain Res. 2008, 1220, 191–198. [Google Scholar] [CrossRef]
- Koelsch, S.; Schröger, E.; Tervaniemi, M. Superior pre-attentive auditory processing in musicians. Neuroreport 1999, 10, 1309–1313. [Google Scholar] [CrossRef]
- Shahin, A.J.; Roberts, L.E.; Chau, W.; Trainor, L.J.; Miller, L.M. Music training leads to the development of timbre-specific gamma band activity. Neuroimage 2008, 41, 113–122. [Google Scholar] [CrossRef]
- Shahin, A.J.; Bosnyak, D.J.; Trainor, L.J.; Roberts, L.E. Enhancement of neuroplastic P2 and N1c auditory evoked potentials in musicians. J. Neurosci. 2003, 23, 5545–5552. [Google Scholar] [CrossRef]
- Strait, D.L.; Kraus, N.; Skoe, E.; Ashley, R. Musical experience and neural efficiency: Effects of training on subcortical processing of vocal expressions of emotion. Eur. J. Neurosci. 2009, 29, 661–668. [Google Scholar] [CrossRef] [PubMed]
- Pantev, C.; Oostenveld, R.; Engelien, A.; Ross, B.; Roberts, L.E.; Hoke, M. Increased auditory cortical representation in musicians. Nature 1998, 392, 811–814. [Google Scholar] [CrossRef] [PubMed]
- Shahin, A.J.; Roberts, L.E.; Pantev, C.; Trainor, L.J.; Ross, B. Modulation of P2 auditory-evoked responses by the spectral complexity of musical sounds. Neuroreport 2005, 16, 1781–1785. [Google Scholar] [CrossRef] [PubMed]
- Lütkenhöner, B.; Seither-Preisler, A.; Seither, S. Piano tones evoke stronger magnetic fields than pure tones or noise, both in musicians and non-musicians. Neuroimage 2006, 30, 927–937. [Google Scholar] [CrossRef] [PubMed]
- Besson, M.; Schön, D.; Moreno, S.; Santos, A.; Magne, C. Influence of musical expertise and musical training on pitch processing in music and language. Restor. Neurol. Neurosci. 2007, 25, 399–410. [Google Scholar]
- Kaganovich, N.; Kim, J.; Herring, C.; Schumaker, J.; Macpherson, M.; Weber-Fox, C. Musicians show general enhancement of complex sound encoding and better inhibition of irrelevant auditory change in music: An ERP study. Eur. J. Neurosci. 2013, 37, 1295–1307. [Google Scholar] [CrossRef]
- Schön, D.; Magne, C.; Besson, M. The music of speech: Music training facilitates pitch processing in both music and language. Psychophysiology 2004, 41, 341–349. [Google Scholar] [CrossRef]
- Rigoulot, S.; Pell, M.D.; Armony, J.L. Time course of the influence of musical expertise on the processing of vocal and musical sounds. Neuroscience 2015, 290, 175–184. [Google Scholar] [CrossRef]
- Pinheiro, A.P.; Vasconcelos, M.; Dias, M.; Arrais, N.; Gonçalves, Ó.F. The music of language: An ERP investigation of the effects of musical training on emotional prosody processing. Brain Lang 2015, 140, 24–34. [Google Scholar] [CrossRef]
- Nolden, S.; Rigoulot, S.; Jolicoeur, P.; Armony, J.L. Effects of musical expertise on oscillatory brain activity in response to emotional sounds. Neuropsychologia 2017, 103, 96–105. [Google Scholar] [CrossRef]
- Martins, I.; Lima, C.F.; Pinheiro, A.P. Enhanced salience of musical sounds in singers and instrumentalists. Cogn. Affect Behav. Neurosci. 2022, 22, 1044–1062. [Google Scholar] [CrossRef] [PubMed]
- Frühholz, S.; Klaas, H.S.; Patel, S.; Grandjean, D. Talking in Fury: The Cortico-Subcortical Network Underlying Angry Vocalizations. Cereb. Cortex 2015, 25, 2752–2762. [Google Scholar] [CrossRef] [PubMed]
- Kawahara, H.; Morise, M.; Takahashi, T.; Nisimura, R.; Irino, T.; Banno, H. TANDEM-STRAIGHT: A temporally stable power spectral representation for periodic signals and applications to interference-free spectrum, F0, and aperiodicity estimation. In Proceedings of the IEEE International Conference on Acoustics, Speech and Signal Processing, Las Vegas, NV, USA, 31 March–4 April 2008. [Google Scholar]
- Kawahara, H.; Skuk, V.G. Voice Morphing. In The Oxford Handbook of Voice Perception; Frühholz, S., Belin, P., Frühholz, S., Belin, P., Scherer, K.R., Eds.; Oxford University Press: Oxford, UK, 2018; pp. 684–706. ISBN 9780198743187. [Google Scholar]
- Nussbaum, C.; Pöhlmann, M.; Kreysa, H.; Schweinberger, S.R. Perceived naturalness of emotional voice morphs. Cogn. Emot. 2023, 37, 731–747. [Google Scholar] [CrossRef] [PubMed]
- Boersma, P. Praat: Doing Phonetics by Computer [Computer Program]: Version 6.0.46. 2018. Available online: http://www.praat.org/ (accessed on 25 January 2020).
- Kang, K.; Schneider, D.; Schweinberger, S.R.; Mitchell, P. Dissociating neural signatures of mental state retrodiction and classification based on facial expressions. Soc. Cogn. Affect. Neurosci. 2018, 13, 933–943. [Google Scholar] [CrossRef] [PubMed]
- Psychology Software Tools, Inc. E-Prime 3.0; Pittsburgh, PA. 2016. Available online: https://support.pstnet.com/ (accessed on 25 September 2023).
- Watson, D.; Clark, L.A.; Tellegen, A. Development and validation of brief measures of positive and negative affect: The PANAS scales. J. Pers. Soc. Psychol. 1988, 54, 1063–1070. [Google Scholar] [CrossRef] [PubMed]
- Rammstedt, B.; Danner, D.; Soto, C.J.; John, O.P. Validation of the short and extra-short forms of the Big Five Inventory-2 (BFI-2) and their German adaptations. Eur. J. Psychol. Assess. 2018, 36, 149–161. [Google Scholar] [CrossRef]
- Müllensiefen, D.; Gingras, B.; Musil, J.; Stewart, L. The musicality of non-musicians: An index for assessing musical sophistication in the general population. PLoS ONE 2014, 9, e89642. [Google Scholar] [CrossRef]
- Freitag, C.M.; Retz-Junginger, P.; Retz, W.; Seitz, C.; Palmason, H.; Meyer, J.; Rösler, M.; Gontard, A. von. Evaluation der deutschen Version des Autismus-Spektrum-Quotienten (AQ)—Die Kurzversion AQ-k. Z. Für Klin. Psychol. Und Psychother. 2007, 36, 280–289. [Google Scholar] [CrossRef]
- Breyer, B.; Bluemke, M. Deutsche Version der Positive and Negative Affect Schedule PANAS (GESIS Panel); GESIS—Leibniz-Institut für Sozialwissenschaften: Mannheim, Germany, 2016. [Google Scholar]
- Baron-Cohen, S.; Wheelwright, S.; Skinner, R.; Martin, J.-C.; Clubley, E. The autism-spectrum quotient (AQ): Evidence from asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J. Autism Dev. Disord. 2001, 31, 5–17. [Google Scholar] [CrossRef]
- Law, L.N.C.; Zentner, M. Assessing musical abilities objectively: Construction and validation of the profile of music perception skills. PLoS ONE 2012, 7, e52508. [Google Scholar] [CrossRef]
- Zentner, M.; Strauss, H. Assessing musical ability quickly and objectively: Development and validation of the Short-PROMS and the Mini-PROMS. Ann. N. Y. Acad. Sci. 2017, 1400, 33–45. [Google Scholar] [CrossRef] [PubMed]
- Delorme, A.; Makeig, S. EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 2004, 134, 9–21. [Google Scholar] [CrossRef] [PubMed]
- MATLAB; Version 9.8.0 (R2020a); The MathWorks Inc.: Natick, MA, USA, 2020.
- Freeden, W. Spherical spline interpolation—Basic theory and computational aspects. J. Comput. Appl. Math. 1984, 11, 367–375. [Google Scholar] [CrossRef]
- Kayser, J. Current Source Density (CSD) Interpolation Using Spherical Splines-Csd Toolbox. Division of Cognitive Neuroscience. New York State Psychiatric Institute. 2009. Available online: https://psychophysiology.cpmc.columbia.edu/software/CSDtoolbox/index.html (accessed on 25 September 2023).
- Kayser, J.; Tenke, C.E. On the benefits of using surface Laplacian (current source density) methodology in electrophysiology. Int. J. Psychophysiol. 2015, 97, 171–173. [Google Scholar] [CrossRef] [PubMed]
- Hajcak, G.; Foti, D. Significance? Significance! Empirical, methodological, and theoretical connections between the late positive potential and P300 as neural responses to stimulus significance: An integrative review. Psychophysiology 2020, 57, e13570. [Google Scholar] [CrossRef]
- R Core Team. R: A Language and Environment for Statistical Computing; R Core Team: Vienna, Austria, 2020; Available online: https://www.R-project.org/ (accessed on 25 September 2023).
- Kroes, A.D.A.; Finley, J.R. Demystifying omega squared: Practical guidance for effect size in common analysis of variance designs. Psychol. Methods, 2023; online ahead of print. [Google Scholar] [CrossRef]
- Fritz, C.O.; Morris, P.E.; Richler, J.J. Effect size estimates: Current use, calculations, and interpretation. J. Exp. Psychol. Gen. 2012, 141, 2–18. [Google Scholar] [CrossRef]
- Park, M.; Gutyrchik, E.; Welker, L.; Carl, P.; Pöppel, E.; Zaytseva, Y.; Meindl, T.; Blautzik, J.; Reiser, M.; Bao, Y. Sadness is unique: Neural processing of emotions in speech prosody in musicians and non-musicians. Front. Hum. Neurosci. 2015, 8, 1049. [Google Scholar] [CrossRef]
- Schirmer, A.; Croy, I.; Schweinberger, S.R. Social touch—A tool rather than a signal. Curr. Opin. Behav. Sci. 2022, 44, 101100. [Google Scholar] [CrossRef]
- Milovanov, R.; Huotilainen, M.; Esquef, P.A.A.; Alku, P.; Välimäki, V.; Tervaniemi, M. The role of musical aptitude and language skills in preattentive duration processing in school-aged children. Neurosci. Lett. 2009, 460, 161–165. [Google Scholar] [CrossRef]
- Partanen, E.; Kivimäki, R.; Huotilainen, M.; Ylinen, S.; Tervaniemi, M. Musical perceptual skills, but not neural auditory processing, are associated with better reading ability in childhood. Neuropsychologia 2022, 169, 108189. [Google Scholar] [CrossRef]
- Santoyo, A.E.; Gonzales, M.G.; Iqbal, Z.J.; Backer, K.C.; Balasubramaniam, R.; Bortfeld, H.; Shahin, A.J. Neurophysiological time course of timbre-induced music-like perception. J. Neurophysiol. 2023, 130, 291–302. [Google Scholar] [CrossRef] [PubMed]
- Zäske, R.; Volberg, G.; Kovács, G.; Schweinberger, S.R. Electrophysiological correlates of voice learning and recognition. J. Neurosci. 2014, 34, 10821–10831. [Google Scholar] [CrossRef] [PubMed]
- Petit, S.; Badcock, N.A.; Grootswagers, T.; Woolgar, A. Unconstrained multivariate EEG decoding can help detect lexical-semantic processing in individual children. Sci. Rep. 2020, 10, 10849. [Google Scholar] [CrossRef] [PubMed]
P200 | N400 | LPP | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
df1|2 | F | p | Ωp2 | F | p | Ωp2 | F | p | Ωp2 | |
Group | 1|76 | 0.78 | 0.380 | <0.01 | 0.04 | 0.848 | <0.01 | 2.15 | 0.147 | 0.03 |
Emotion (Emo) | 3|228 | 1.52 | 0.211 | <0.01 | 6.96 | <0.001 | 0.084 | 5.24 | 0.002 | 0.07 |
Morph Type (MType) | 2|152 | 0.13 | 0.882 | 0.1 | 3.80 | 0.024 | 0.048 | 8.18 | <0.001 | 0.10 |
Group × Emo | 3|228 | 0.55 | 0.651 | <0.01 | 0.51 | 0.679 | 0.017 | 1.71 | 0.166 | 0.02 |
Group × Mtype | 2|152 | 1.04 | 0.356 | <0.01 | 0.18 | 0.832 | <0.01 | 0.23 | 0.791 | <0.01 |
Emo × Mtype | 6|456 | 3.80 | 0.001 | 0.04 | 5.44 | <0.001 | 0.067 | 1.58 | 0.156 | 0.02 |
Group × Emo × Mtype | 6|456 | 1.01 | 0.416 | <0.01 | 0.83 | 0.548 | 0.1 | 2.49 | 0.025 | 0.03 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Nussbaum, C.; Schirmer, A.; Schweinberger, S.R. Electrophysiological Correlates of Vocal Emotional Processing in Musicians and Non-Musicians. Brain Sci. 2023, 13, 1563. https://doi.org/10.3390/brainsci13111563
Nussbaum C, Schirmer A, Schweinberger SR. Electrophysiological Correlates of Vocal Emotional Processing in Musicians and Non-Musicians. Brain Sciences. 2023; 13(11):1563. https://doi.org/10.3390/brainsci13111563
Chicago/Turabian StyleNussbaum, Christine, Annett Schirmer, and Stefan R. Schweinberger. 2023. "Electrophysiological Correlates of Vocal Emotional Processing in Musicians and Non-Musicians" Brain Sciences 13, no. 11: 1563. https://doi.org/10.3390/brainsci13111563
APA StyleNussbaum, C., Schirmer, A., & Schweinberger, S. R. (2023). Electrophysiological Correlates of Vocal Emotional Processing in Musicians and Non-Musicians. Brain Sciences, 13(11), 1563. https://doi.org/10.3390/brainsci13111563