Tension-Related Activity in the Orbitofrontal Cortex and Amygdala
Tension-Related Activity in the Orbitofrontal Cortex and Amygdala
Tonal music is characterized by a continuous flow of tension and resolution. This flow of tension and resolution is closely related to processes of expectancy and prediction and is a key mediator of music-evoked emotions. However, the neural correlates of subjectively experienced tension and resolution have not yet been investigated. We acquired continuous ratings of musical tension for four piano pieces. In a subsequent functional magnetic resonance imaging experiment, we identified blood oxygen level-dependent signal increases related to musical tension in the left lateral orbitofrontal cortex (pars orbitalis of the inferior frontal gyrus). In addition, a region of interest analysis in bilateral amygdala showed activation in the right superficial amygdala during periods of increasing tension (compared with decreasing tension). This is the first neuroimaging study investigating the time-varying changes of the emotional experience of musical tension, revealing brain activity in key areas of affective processing.
The processing of music involves a complex machinery of cognitive and affective functions that rely on neurobiological processes of the human brain (Peretz and Zatorre, 2005; Koelsch, 2012; Pearce and Rohrmeier, 2012). The past years have seen a growing interest in using music as a tool to study these functions and their underlying neuronal mechanisms (Zatorre, 2005). Because of its power to evoke strong emotional experiences, music is particularly interesting for affective neuroscience, and an increasing number of neuroimaging studies use music to unveil the brain mechanisms underlying emotion (for reviews see Koelsch, 2010; Peretz, 2010). Corresponding research has shown that music-evoked emotions modulate neural responses in a variety of limbic and paralimbic brain areas that are also activated during emotional experiences in other contexts. For example, pleasant emotional responses to music are associated with the activation of the mesolimbic reward system (Blood and Zatorre, 2001; Menon and Levitin, 2005; Salimpoor et al., 2011) that also responds to stimuli of more direct biological reward value such as food or sex (Berridge, 2003). Music thus appears to recruit evolutionarily ancient brain circuits associated with fundamental aspects of affective behaviour, and research on music-evoked emotion is therefore not only relevant for music psychology but promises new insights into general mechanisms underlying emotion.
Furthermore, because music unfolds over time, it is especially well-suited to studying the dynamic, time-varying aspects of emotional experience. These continuous fluctuations of emotional experience have been largely neglected by neuroimaging research on emotions, which predominantly has focused on more stationary aspects of affective experience during short emotional episodes. Corresponding studies, for example, investigated discrete emotions (such as happiness, sadness, anger, or fear) or emotional valence (pleasant vs unpleasant) in response to static experimental stimuli such as facial expressions (Breiter et al., 1996; Morris et al., 1996; Blair et al., 1999), affective pictures (Liberzon et al., 2003; Taylor et al., 2003; Phan et al., 2004), or words (Maddock et al., 2003; Kuchinke et al., 2005). Likewise, the focus on static aspects of emotions is also reflected in neuroimaging studies on music-evoked emotions, which generally assume that an emotional response to a piece of music remains relatively constant over the entire duration of the piece. Neural correlates of music-evoked emotions have, for example, been investigated by contrasting consonant/dissonant (Blood et al., 1999), pleasant/unpleasant (Koelsch et al., 2006), or happy/sad (Khalfa et al., 2005; Mitterschiffthaler et al., 2007) music stimuli, or by comparing different emotion dimensions (e.g. nostalgia, power, or peacefulness) of short music excerpts (Trost et al., 2012). However, emotions are rarely static states, and their dynamic, time-varying nature is in fact one of their defining features (Scherer, 2005). These dynamic fluctuations of emotional experience are poorly captured by fixed emotion labels globally attributed to an experimental stimulus (like happy vs sad, or pleasant vs unpleasant). Using music to investigate the temporal fluctuations of affective experiences can, therefore, provide new insights into mechanisms of neuro-affective processing.
A few studies have begun to investigate dynamic changes of emotions and their underlying brain mechanisms by using continuous self-report methods (Nagel et al., 2007; Schubert, 2010), in which emotions are continuously tracked over time. Chapin et al. (2010), for example, investigated neural correlates of emotional arousal during a Chopin étude in a functional magnetic resonance imaging (fMRI) study, and Mikutta et al. (2012) used arousal ratings for Beethoven's fifth symphony to investigate their relation to different frequency bands in the electroencephalogram. In the film domain, Goldin et al. (2005) used continuous ratings of emotional intensity to uncover brain activations in response to sad and amusing film clips that were not detected by conventional block contrasts. Similarly, Wallentin et al. (2011) identified brain activations in language and emotion areas (temporal cortices, left inferior frontal gyrus (IFG), amygdala and motor cortices) related to continuous ratings of emotional intensity and valence during story comprehension.
This study aims to extend previous research by using musical tension to investigate the dynamic change of emotional experience over the course of a musical piece. Musical tension refers to the continuous ebb and flow of tension and resolution that is usually experienced when listening to a piece of Western tonal music. In particular, tension is triggered by expectancies that are caused by implication relationships between musical events, which are implicitly acquired through exposure to a musical system (Rohrmeier and Rebuschat, 2012). For example, a musical event that sets up harmonic implications, such as an unstable dominant seventh chord, may build up tension, which is finally resolved by the occurrence of an implied event, such as a stable tonic chord. The implicative relationships can be local or non-local, i.e. the implicative and implied events do not necessarily have to follow each other directly but may stretch over long distances and can be recursively nested (cf. Lerdahl, 2004; Rohrmeier, 2011). Thus, prediction and expectancy, which have been proposed as one key mechanism of emotion elicitation in music (Meyer, 1956; Huron, 2006; Juslin and Västfjäll, 2008; Koelsch, 2012), are inherently linked to musical tension (other factors related to tension are, e.g. consonance/dissonance, stability/instability and suspense emerging from large-scale structures; for details see Lehne and Koelsch, in press). The pertinent expectancy and prediction processes are not only relevant for music processing (for reviews see Fitch et al., 2009; Pearce and Wiggins, 2012; Rohrmeier and Koelsch, 2012) but have been proposed as a fundamental mechanism underlying human cognition (Gregory, 1980; Dennett, 1996) and brain functioning (Bar, 2007; Bubic et al., 2010; Friston, 2010). Therefore, studying the neural bases of musical tension can shed light on general principles of predictive processing, predictive coding (Friston and Kiebel, 2009) and their connections to dynamic changes of affective experience.
In the music domain, neural processes related to expectancy violations have been studied using short chord sequences that either ended on expected or unexpected chords (e.g. Koelsch et al., 2005; Tillmann et al., 2006). The music-syntactic processing of such expectancy violations has mainly been associated with neural responses in Brodmann area 44 of the inferior fronto-lateral cortex (Koelsch et al., 2005). However, activations in areas related to emotive processing, such as the orbitofrontal cortex (OFC) (Koelsch et al., 2005; Tillmann et al., 2006) and the amygdala (Koelsch et al., 2008a) as well as increases in electrodermal activity (Steinbeis et al., 2006; Koelsch et al., 2008b) indicate that affective processes also play a role in the processing of syntactically irregular events. The affective responses to breaches of expectancy in music were investigated more closely in an fMRI study by Koelsch et al. (2008a) who reported increased activation of the amygdala (superficial group) in response to unexpected chord functions, thus corroborating the link between affective processes and breaches of expectancy.
In this study, we acquired continuous ratings of felt musical tension for a set of ecologically valid music stimuli (four piano pieces by Mendelssohn, Mozart, Schubert and Tchaikovsky), thus extending the more simplistic chord-sequence paradigms of previous studies (Koelsch et al., 2005, 2008a; Steinbeis et al., 2006; Tillmann et al., 2006) to real music. Subsequently, we recorded fMRI data (from the same participants) and used the tension ratings as continuous regressor to identify brain areas related to the time-varying experience of musical tension. In addition, we compared stimulus epochs corresponding to increasing and decreasing tension. Based on the studies reported above (Koelsch et al., 2005, 2008a; Tillmann et al., 2006), we investigated whether musical tension modulates neuronal activity in limbic/paralimbic brain structures known to be involved in emotion processing. We also tested the more specific regional hypothesis that tension is related to activity changes in the amygdala, assuming that structural breaches of expectancy are key to the elicitation of tension (Meyer, 1956; Koelsch, 2012), and that such breaches of expectancy modulate amygdala activity as reported in the study by Koelsch et al. (2008a).
Abstract and Introduction
Abstract
Tonal music is characterized by a continuous flow of tension and resolution. This flow of tension and resolution is closely related to processes of expectancy and prediction and is a key mediator of music-evoked emotions. However, the neural correlates of subjectively experienced tension and resolution have not yet been investigated. We acquired continuous ratings of musical tension for four piano pieces. In a subsequent functional magnetic resonance imaging experiment, we identified blood oxygen level-dependent signal increases related to musical tension in the left lateral orbitofrontal cortex (pars orbitalis of the inferior frontal gyrus). In addition, a region of interest analysis in bilateral amygdala showed activation in the right superficial amygdala during periods of increasing tension (compared with decreasing tension). This is the first neuroimaging study investigating the time-varying changes of the emotional experience of musical tension, revealing brain activity in key areas of affective processing.
Introduction
The processing of music involves a complex machinery of cognitive and affective functions that rely on neurobiological processes of the human brain (Peretz and Zatorre, 2005; Koelsch, 2012; Pearce and Rohrmeier, 2012). The past years have seen a growing interest in using music as a tool to study these functions and their underlying neuronal mechanisms (Zatorre, 2005). Because of its power to evoke strong emotional experiences, music is particularly interesting for affective neuroscience, and an increasing number of neuroimaging studies use music to unveil the brain mechanisms underlying emotion (for reviews see Koelsch, 2010; Peretz, 2010). Corresponding research has shown that music-evoked emotions modulate neural responses in a variety of limbic and paralimbic brain areas that are also activated during emotional experiences in other contexts. For example, pleasant emotional responses to music are associated with the activation of the mesolimbic reward system (Blood and Zatorre, 2001; Menon and Levitin, 2005; Salimpoor et al., 2011) that also responds to stimuli of more direct biological reward value such as food or sex (Berridge, 2003). Music thus appears to recruit evolutionarily ancient brain circuits associated with fundamental aspects of affective behaviour, and research on music-evoked emotion is therefore not only relevant for music psychology but promises new insights into general mechanisms underlying emotion.
Furthermore, because music unfolds over time, it is especially well-suited to studying the dynamic, time-varying aspects of emotional experience. These continuous fluctuations of emotional experience have been largely neglected by neuroimaging research on emotions, which predominantly has focused on more stationary aspects of affective experience during short emotional episodes. Corresponding studies, for example, investigated discrete emotions (such as happiness, sadness, anger, or fear) or emotional valence (pleasant vs unpleasant) in response to static experimental stimuli such as facial expressions (Breiter et al., 1996; Morris et al., 1996; Blair et al., 1999), affective pictures (Liberzon et al., 2003; Taylor et al., 2003; Phan et al., 2004), or words (Maddock et al., 2003; Kuchinke et al., 2005). Likewise, the focus on static aspects of emotions is also reflected in neuroimaging studies on music-evoked emotions, which generally assume that an emotional response to a piece of music remains relatively constant over the entire duration of the piece. Neural correlates of music-evoked emotions have, for example, been investigated by contrasting consonant/dissonant (Blood et al., 1999), pleasant/unpleasant (Koelsch et al., 2006), or happy/sad (Khalfa et al., 2005; Mitterschiffthaler et al., 2007) music stimuli, or by comparing different emotion dimensions (e.g. nostalgia, power, or peacefulness) of short music excerpts (Trost et al., 2012). However, emotions are rarely static states, and their dynamic, time-varying nature is in fact one of their defining features (Scherer, 2005). These dynamic fluctuations of emotional experience are poorly captured by fixed emotion labels globally attributed to an experimental stimulus (like happy vs sad, or pleasant vs unpleasant). Using music to investigate the temporal fluctuations of affective experiences can, therefore, provide new insights into mechanisms of neuro-affective processing.
A few studies have begun to investigate dynamic changes of emotions and their underlying brain mechanisms by using continuous self-report methods (Nagel et al., 2007; Schubert, 2010), in which emotions are continuously tracked over time. Chapin et al. (2010), for example, investigated neural correlates of emotional arousal during a Chopin étude in a functional magnetic resonance imaging (fMRI) study, and Mikutta et al. (2012) used arousal ratings for Beethoven's fifth symphony to investigate their relation to different frequency bands in the electroencephalogram. In the film domain, Goldin et al. (2005) used continuous ratings of emotional intensity to uncover brain activations in response to sad and amusing film clips that were not detected by conventional block contrasts. Similarly, Wallentin et al. (2011) identified brain activations in language and emotion areas (temporal cortices, left inferior frontal gyrus (IFG), amygdala and motor cortices) related to continuous ratings of emotional intensity and valence during story comprehension.
This study aims to extend previous research by using musical tension to investigate the dynamic change of emotional experience over the course of a musical piece. Musical tension refers to the continuous ebb and flow of tension and resolution that is usually experienced when listening to a piece of Western tonal music. In particular, tension is triggered by expectancies that are caused by implication relationships between musical events, which are implicitly acquired through exposure to a musical system (Rohrmeier and Rebuschat, 2012). For example, a musical event that sets up harmonic implications, such as an unstable dominant seventh chord, may build up tension, which is finally resolved by the occurrence of an implied event, such as a stable tonic chord. The implicative relationships can be local or non-local, i.e. the implicative and implied events do not necessarily have to follow each other directly but may stretch over long distances and can be recursively nested (cf. Lerdahl, 2004; Rohrmeier, 2011). Thus, prediction and expectancy, which have been proposed as one key mechanism of emotion elicitation in music (Meyer, 1956; Huron, 2006; Juslin and Västfjäll, 2008; Koelsch, 2012), are inherently linked to musical tension (other factors related to tension are, e.g. consonance/dissonance, stability/instability and suspense emerging from large-scale structures; for details see Lehne and Koelsch, in press). The pertinent expectancy and prediction processes are not only relevant for music processing (for reviews see Fitch et al., 2009; Pearce and Wiggins, 2012; Rohrmeier and Koelsch, 2012) but have been proposed as a fundamental mechanism underlying human cognition (Gregory, 1980; Dennett, 1996) and brain functioning (Bar, 2007; Bubic et al., 2010; Friston, 2010). Therefore, studying the neural bases of musical tension can shed light on general principles of predictive processing, predictive coding (Friston and Kiebel, 2009) and their connections to dynamic changes of affective experience.
In the music domain, neural processes related to expectancy violations have been studied using short chord sequences that either ended on expected or unexpected chords (e.g. Koelsch et al., 2005; Tillmann et al., 2006). The music-syntactic processing of such expectancy violations has mainly been associated with neural responses in Brodmann area 44 of the inferior fronto-lateral cortex (Koelsch et al., 2005). However, activations in areas related to emotive processing, such as the orbitofrontal cortex (OFC) (Koelsch et al., 2005; Tillmann et al., 2006) and the amygdala (Koelsch et al., 2008a) as well as increases in electrodermal activity (Steinbeis et al., 2006; Koelsch et al., 2008b) indicate that affective processes also play a role in the processing of syntactically irregular events. The affective responses to breaches of expectancy in music were investigated more closely in an fMRI study by Koelsch et al. (2008a) who reported increased activation of the amygdala (superficial group) in response to unexpected chord functions, thus corroborating the link between affective processes and breaches of expectancy.
In this study, we acquired continuous ratings of felt musical tension for a set of ecologically valid music stimuli (four piano pieces by Mendelssohn, Mozart, Schubert and Tchaikovsky), thus extending the more simplistic chord-sequence paradigms of previous studies (Koelsch et al., 2005, 2008a; Steinbeis et al., 2006; Tillmann et al., 2006) to real music. Subsequently, we recorded fMRI data (from the same participants) and used the tension ratings as continuous regressor to identify brain areas related to the time-varying experience of musical tension. In addition, we compared stimulus epochs corresponding to increasing and decreasing tension. Based on the studies reported above (Koelsch et al., 2005, 2008a; Tillmann et al., 2006), we investigated whether musical tension modulates neuronal activity in limbic/paralimbic brain structures known to be involved in emotion processing. We also tested the more specific regional hypothesis that tension is related to activity changes in the amygdala, assuming that structural breaches of expectancy are key to the elicitation of tension (Meyer, 1956; Koelsch, 2012), and that such breaches of expectancy modulate amygdala activity as reported in the study by Koelsch et al. (2008a).
