Eyes Wide Shut: Amygdala Mediates Eyes-Closed Effect on Emotional Experience with Music

University of Leuven, Belgium
PLoS ONE (Impact Factor: 3.23). 02/2009; 4(7):e6230. DOI: 10.1371/journal.pone.0006230
Source: PubMed


The perceived emotional value of stimuli and, as a consequence the subjective emotional experience with them, can be affected by context-dependent styles of processing. Therefore, the investigation of the neural correlates of emotional experience requires accounting for such a variable, a matter of an experimental challenge. Closing the eyes affects the style of attending to auditory stimuli by modifying the perceptual relationship with the environment without changing the stimulus itself. In the current study, we used fMRI to characterize the neural mediators of such modification on the experience of emotionality in music. We assumed that closed eyes position will reveal interplay between different levels of neural processing of emotions. More specifically, we focused on the amygdala as a central node of the limbic system and on its co-activation with the Locus Ceruleus (LC) and Ventral Prefrontal Cortex (VPFC); regions involved in processing of, respectively, 'low', visceral-, and 'high', cognitive-related, values of emotional stimuli. Fifteen healthy subjects listened to negative and neutral music excerpts with eyes closed or open. As expected, behavioral results showed that closing the eyes while listening to emotional music resulted in enhanced rating of emotionality, specifically of negative music. In correspondence, fMRI results showed greater activation in the amygdala when subjects listened to the emotional music with eyes closed relative to eyes open. More so, by using voxel-based correlation and a dynamic causal model analyses we demonstrated that increased amygdala activation to negative music with eyes closed led to increased activations in the LC and VPFC. This finding supports a system-based model of perceived emotionality in which the amygdala has a central role in mediating the effect of context-based processing style by recruiting neural operations involved in both visceral (i.e. 'low') and cognitive (i.e. 'high') related processes of emotions.

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    • "Visual imagery is considered as one basic emotion-evoking principle during music listening [68] and anatomical studies indicate that auditory core, belt and parabelt regions project to V1 and V2 of the visual cortex, and that neurons in V2 project back into these auditory regions [69]. Note that the eyes-closed requirement of the experimental task used in the present study was motivated by evidence suggesting that affective activity is enhanced when the eyes are closed [70], a condition that practically minimizes any vision-specific sensory contributions to visual cortex activity. Evidence suggesting that the occipital visual cortex is also involved in spatial hearing, in people with normal sight, have also been observed during several different auditory tasks (for details see 71). "
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    ABSTRACT: The purpose of the present study was the investigation of interaction effects between functional MRI scanner noise and affective neural processes. Stimuli comprised of psychoacoustically balanced musical pieces, expressing three different emotions (fear, neutral, joy). Participants (N=34, 19 female) were split into two groups, one subjected to continuous scanning and another subjected to sparse temporal scanning that features decreased scanner noise. Tests for interaction effects between scanning group (sparse/quieter vs continuous/noisier) and emotion (fear, neutral, joy) were performed. Results revealed interactions between the affective expression of stimuli and scanning group localized in bilateral auditory cortex, insula and visual cortex (calcarine sulcus). Post-hoc comparisons revealed that during sparse scanning, but not during continuous scanning, BOLD signals were significantly stronger for joy than for fear, as well as stronger for fear than for neutral in bilateral auditory cortex. During continuous scanning, but not during sparse scanning, BOLD signals were significantly stronger for joy than for neutral in the left auditory cortex and for joy than for fear in the calcarine sulcus. To the authors' knowledge, this is the first study to show a statistical interaction effect between scanner noise and affective processes and extends evidence suggesting scanner noise to be an important factor in functional MRI research that can affect and distort affective brain processes.
    PLoS ONE 11/2013; 8(11):e80564. DOI:10.1371/journal.pone.0080564 · 3.23 Impact Factor
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    • "Another putative confound constitutes the instruction of keeping eyes closed during stimulus presentation. A recent neuroimaging study showed that closing the eyes while listening to emotional music, resulted in enhanced ratings of emotionality and greater activation of the amygdala (as well as Locus Coeruleus and Ventral Prefrontal Cortex) [56]. Moreover, as compared to healthy controls and patients with obsessive compulsive disorders, DPD patients showed reduced neural activation for affective visual stimuli in regions involved in visual processing (middle and superior temporal gyri), which might reflect lower attention to aversive stimuli [19]. "
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    ABSTRACT: Patients with depersonalization disorder (DPD) typically complain about emotional detachment. Previous studies found reduced autonomic responsiveness to emotional stimuli for DPD patients as compared to patients with anxiety disorders. We aimed to investigate autonomic responsiveness to emotional auditory stimuli of DPD patients as compared to patient controls. Furthermore, we examined the modulatory effect of mindful breathing on these responses as well as on depersonalization intensity. 22 DPD patients and 15 patient controls balanced for severity of depression and anxiety, age, sex and education, were compared regarding 1) electrodermal and heart rate data during a resting period, and 2) autonomic responses and cognitive appraisal of standardized acoustic affective stimuli in two conditions (normal listening and mindful breathing). DPD patients rated the emotional sounds as significantly more neutral as compared to patient controls and standardized norm ratings. At the same time, however, they responded more strongly to acoustic emotional stimuli and their electrodermal response pattern was more modulated by valence and arousal as compared to patient controls. Mindful breathing reduced severity of depersonalization in DPD patients and increased the arousal modulation of electrodermal responses in the whole sample. Finally, DPD patients showed an increased electrodermal lability in the rest period as compared to patient controls. These findings demonstrated that the cognitive evaluation of emotional sounds in DPD patients is disconnected from their autonomic responses to those emotional stimuli. The increased electrodermal lability in DPD may reflect increased introversion and cognitive control of emotional impulses. The findings have important psychotherapeutic implications.
    PLoS ONE 09/2013; 8(9):e74331. DOI:10.1371/journal.pone.0074331 · 3.23 Impact Factor
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    • "An alternative approach was taken by Lerner et al. (2009), which attempted to modulate the level of spontaneous activity by using eyes-open (EO) and eyes-closed (EC) baseline conditions whilst stimuli consisting of musical tones were presented. It was found that the tones induced greater BOLD signal response in the auditory cortex during the EO than the EC condition. "
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    ABSTRACT: Previous studies suggest that there may be a distinct relationship between spontaneous neural activity and subsequent or concurrent self-specific stimulus-induced activity. This study aims to test the impact of spontaneous activity as recorded in an eyes-open (EO) resting state as opposed to eyes-closed (EC) on self-specific versus non-self-specific auditory stimulus-induced activity in fMRI. In our first experiment we used self-specific stimuli comprised of the subject's own name and non-self-specific stimuli comprised of a friend's name and an unknown name, presented during EO versus EC baselines in a 3 name condition × 2 baseline design. In Experiment 2 we directly measured spontaneous activity in the absence of stimuli during EO versus EC to confirm a modulatory effect of the two baseline conditions in the regions found to show an interaction effect in Experiment 1. Spontaneous activity during EO was significantly higher than during EC in bilateral auditory cortex and non-self-specific names yielded stronger signal changes relative to EO baseline than to EC. In contrast, there was no difference in response to self-specific names relative to EO baseline than to EC despite the difference between spontaneous activity levels. These results support an impact of spontaneous activity on stimulus-induced activity, moreover an impact that depends on the high-level stimulus characteristic of self-specificity.
    Frontiers in Human Neuroscience 07/2013; 7:437. DOI:10.3389/fnhum.2013.00437 · 3.63 Impact Factor
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